124. Creighton, MJA; Greenberg, DA; Reader, SM; Mooers, AO. (2021) The role of behavioural flexibility in primate diversification.Anim. Behav. 180: 269-290 The role of behavioural flexibility in primate diversification
behavioural drive; behavioural flexibility; evolutionary diversification; extinction; primate; speciation
Identifying the factors that influence species diversification is fundamental to our understanding of the evolutionary processes underlying extant biodiversity. Behavioural innovation, coupled with the social transmission of new behaviours, has been proposed to increase rates of evolutionary diversification, as novel behaviours expose populations to new selective regimes. Thus, it is believed that behavioural flexibility may be important in driving evolutionary diversification across animals. We test this hypothesis within the primates, a taxonomic group with considerable among-lineage variation in both species diversity and behavioural flexibility. We employ a time cutoff in our phylogeny to help account for biases associated with recent taxonomic reclassifications and compare three alternative measures of diversification rate that consider different phylogenetic depths. We find that the presence of behavioural innovation and social learning are positively correlated with diversification rates among primate genera, but not at shallower phylogenetic depths. Given that we find stronger associations when examining older rather than more recent diversification events, we suggest that extinction resistance, as opposed to speciation, may be an important mechanism linking behavioural flexibility and primate diversification. Our results contrast with work linking behavioural flexibility with diversification of birds at various phylogenetic depths. We offer a possible dispersal-mediated explanation for these conflicting patterns, such that the influence behavioural flexibility plays in dictating evolutionary trajectories differs across clades. Our results suggest that behavioural flexibility may act through several different pathways to shape the evolutionary trajectories of lineages. (c) 2021 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour. DOI
123. Fernandez-Fournier, P; Lewthwaite, JMM; Mooers, AO. (2021) Do We Need to Identify Adaptive Genetic Variation When Prioritizing Populations for Conservation?Conserv. Genet. 22: 205-216 Do We Need to Identify Adaptive Genetic Variation When Prioritizing Populations for Conservation?
Population prioritization; Conservation genomics; GWAS; Adaptive genetic variation; Genetic distinctiveness; NeighborNet
When prioritizing populations for conservation of a given species, it is unclear whether the distribution of standing genetic variation can be used as a suitable proxy for the distribution of useful adaptive genetic variation. We tested whether using genome-wide and putatively adaptive genetic variation give similar prioritization results. We identified adaptive loci via their association with either environmental factors or phenotypic traits using two genomic data sets: yellow warblers (Setophaga petechia) across North America and lodgepole pines (Pinus contorta) in western Canada. We measured pairwise differentiation among populations using a principal components analysis and used a phylogenetic approach (NeighborNet networks) coupled with a measure of evolutionary distinctiveness (Shapley value) to attribute a priority rank to each population. Overall, we found that prioritization rankings using adaptive variation alone were not significantly divergent from rankings based on genome-wide genetic variation. Our testing framework might be of immediate use to conservation practitioners collecting next-generation sequencing data, and we call for further investigation in other species. Our results suggest that we may not need to pursue the contingent step of identifying adaptive variation in species of concern before prioritizing populations, i.e. a naive approach of using genome-wide genetic variation might be a suitable proxy for identifying local adaptation. DOI
122. Gibson, K; Olofsson, J; Mooers, AO; Monroe, MJ. (2021) Pulse grazing by reindeer (Rangifer tarandus) can increase the phylogenetic diversity of vascular plant communities in the Fennoscandian tundra.Ecol. Evol. 11: 14598-14614 Pulse grazing by reindeer (Rangifer tarandus) can increase the phylogenetic diversity of vascular plant communities in the Fennoscandian tundra
biodiversity; community structure; grazing; herbivore; phylogenetic diversity
Herbivore grazing is an important determinant of plant community assemblages. Thus, it is essential to understand its impact to direct conservation efforts in regions where herbivores are managed. While the impacts of reindeer (Rangifer tarandus) grazing on plant biodiversity and community composition in the Fennoscandian tundra are well studied, the impact of reindeer grazing on phylogenetic community structure is not. We used data from a multiyear quasi-experimental study in northern Fennoscandia to analyze the effect of reindeer grazing on plant community diversity including its phylogenetic structure. Our study design used a permanent fence constructed in the 1960s and temporary fences constructed along the permanent fence to expose plant communities to three different grazing regimes: light (almost never grazed), pulse (grazed every other year), and press (chronic grazing for over 40 years). Similar to previous studies on low productivity ecosystems in this region, the species richness and evenness of plant communities with pulse and press grazing did not differ from communities with light grazing. Also consistent with previous studies in this region, we observed a transition from shrub-dominated communities with light grazing to graminoid-dominated communities with pulse and press grazing. Interestingly, communities with pulse, but not press, grazing were more phylogenetically dispersed than communities with light grazing. If grazing pulses can increase the phylogenetic diversity of plant communities, our result suggests changes in reindeer management allowing for pulses of grazing to increase phylogenetic diversity of plant communities. DOI PubMed
121. Greenberg, DA; Pyron, RA; Johnson, LGW; Upham, NS; Jetz, W; Mooers, AO. (2021) Evolutionary legacies in contemporary tetrapod imperilment.Ecol. Lett. 24: 2464-2476 Evolutionary legacies in contemporary tetrapod imperilment
diversification; evolutionary age; extinction risk; extinction selectivity; phylogenetics; range dynamics; turnover; vertebrates
The Tree of Life will be irrevocably reshaped as anthropogenic extinctions continue to unfold. Theory suggests that lineage evolutionary dynamics, such as age since origination, historical extinction filters and speciation rates, have influenced ancient extinction patterns - but whether these factors also contribute to modern extinction risk is largely unknown. We examine evolutionary legacies in contemporary extinction risk for over 4000 genera, representing similar to 30,000 species, from the major tetrapod groups: amphibians, birds, turtles and crocodiles, squamate reptiles and mammals. We find consistent support for the hypothesis that extinction risk is elevated in lineages with higher recent speciation rates. We subsequently test, and find modest support for, a primary mechanism driving this pattern: that rapidly diversifying clades predominantly comprise range-restricted, and extinction-prone, species. These evolutionary patterns in current imperilment may have important consequences for how we manage the erosion of biological diversity across the Tree of Life. DOI PubMed
119. Guzman, LM; Johnson, SA; Mooers, AO; M'Gonigle, LK. (2021) Using historical data to estimate bumble bee occurrence: Variable trends across species provide little support for community-level declines.Biol. Conserv. 257 Using historical data to estimate bumble bee occurrence: Variable trends across species provide little support for community-level declines
Occupancy models; Bumble bees& nbsp; species' declines
Bumble bees are globally important pollinators, especially in temperate regions, and evidence suggests that many species are declining. One recent high profile study by Soroye et al. (2020) applied occupancy models to dated historical collection data to quantify declines across North America and Europe. The authors modelled 66 species across a set of sites spanning both North America and Europe, rather than confining species to sites where they might be expected to occur. In addition, they inferred non-detections for time intervals where there is no evidence that the site was visited (by forcing every site to have exactly 3 visits in each era). We use simulated data to (i) investigate the validity of methods used in that study and (ii) test whether a multi-species framework that incorporates species' ranges and site visitation histories produces better estimates. We show that the method used by Soroye et al. (2020) yields biased estimates of declines, whereas our framework does not. We use such a model to provide revised and appreciably lower estimates for bumble bee community declines, with speciesspecific trends more closely matching classifications from IUCN. The species level trends we provide can help inform future species-at-risk assessments. Well-parameterized occupancy models may be a powerful tool for assessing species-wide trends using curated historical collection data. DOI
118. Higgins, K; Guerrel, J; Lassiter, E; Mooers, A; Palen, WJ; Ibanez, R. (2021) Observations on spindly leg syndrome in a captive population of Andinobates geminisae.Zoo Biol. 40: 330-341 Observations on spindly leg syndrome in a captive population of Andinobates geminisae
amphibian calcium metabolism; amphibian captive husbandry; amphibian health; Andinobates geminisae; Anura; bone development; captive breeding; Dendrobatidae; metamorphosis; spindly leg syndrome (SLS); tadpole
Amphibian health problems of unknown cause limit the success of the growing number of captive breeding programs. Spindly leg syndrome (SLS) is one such disease, where affected individuals with underdeveloped limbs often require euthanization. We experimentally evaluated husbandry-related factors of SLS in a captive population of the critically endangered frog, Andinobates geminisae. SLS has been linked to tadpole nutrition, vitamin B deficiency, water filtration methods, and water quality, but few of these have been experimentally tested. We tested the effects of water filtration method and vitamin supplementation (2017) and the effects of tadpole husbandry protocol intensity (2018) on time to metamorphosis and the occurrence of SLS. We found that vitamin supplementation and reconstituted reverse osmosis filtration of tadpole rearing water significantly reduced SLS prevalence and that reduced tadpole husbandry delayed time to metamorphosis. A fortuitous accident in 2018 resulted in a decrease in the phosphate content of rearing water, which afforded us an additional opportunity to assess the influence of phosphate on calcium sequestration. We found that tadpoles that had more time to sequester calcium for ossification during development had decreased the prevalence of SLS. Taken together, our results suggest that the qualities of the water used to rear tadpoles plays an important role in the development of SLS. Specifically, filtration method, vitamin supplementation, and calcium availability of tadpole rearing water may play important roles. Focused experiments are still needed, but our findings provide important information for amphibian captive rearing programs affected by high SLS prevalence. DOI PubMed
117.Mooers, A; Tucker, CM. (2021) Useful plants have deep evolutionary roots.Nat. Ecol. Evol. 5: 558-559 Useful plants have deep evolutionary roots
It has long been asserted that samples of taxa that span more of the Tree of Life contain more features that humans find useful. This has now been tested at a global scale: across 13,500 plant genera and nearly 9,500 uses, the prediction holds, supporting a macroevolutionary perspective on biodiversity conservation. DOI PubMed
116. Solis-Sosa, R; Mooers, AO; Larrivee, M; Cox, S; Semeniuk, CAD. (2021) A Landscape-Level Assessment of Restoration Resource Allocation for the Eastern Monarch Butterfly.Front. Environ. Sci. 9 A Landscape-Level Assessment of Restoration Resource Allocation for the Eastern Monarch Butterfly
Monarch Butterfly; resource allocation; population modelling; systems dynamics; metapopulation; milkweed; conservation; habitat restoration
The Monarch butterfly eastern population (Danaus plexippus) is in decline primarily due to habitat loss. Current habitat restoration programs focus on re-establishing milkweed, the primary food resource for Monarch caterpillars, in the central United States of America. However, individual components of the Monarch life cycle function as part of an integrated whole. Here we develop the MOBU-SDyM, a migration-wide systems dynamics model of the Monarch butterfly migratory cycle to explore alternative management strategies' impacts. Our model offers several advances over previous efforts, considering complex variables such as dynamic temperature-dependent developmental times, dynamic habitat availability, and weather-related mortality across the entire range. We first explored whether the predominant focus of milkweed restoration in the mid-range of the Monarch's migration could be overestimating the Monarch's actual habitat requirements. Second, we examined the robustness of using the recommended 1.2-1.6 billion milkweed stems as a policy objective when accounting for factors such as droughts, changes in temperature, and the stems' effective usability by the Monarchs. Third, we used the model to estimate the number and distribution of stems across the northern, central, and southern regions of the breeding range needed to reach a self-sustainable long-term Monarch population of six overwintering hectares. Our analysis revealed that concentrating milkweed growth in the central region increases the size of the overwintering colonies more so than equivalent growth in the south region, with growth in the northern region having a negligible effect. However, even though simulating an increase in milkweed stems in the south did not play a key role in increasing the size of the overwintering colonies, it plays a paramount role in keeping the population above a critically small size. Abiotic factors considerably influenced the actual number of stems needed, but, in general, our estimates of required stems were 43-91% larger than the number of stems currently set as a restoration target: our optimal allocation efforts were 7.35, 92, and 0.15% to the south, central, and northern regions, respectively. Systems dynamics' analytical and computational strengths provided us with new avenues to investigate the Monarch's migration as a complex biological system and to contribute to more robust restoration policies for this unique species. DOI
115. Wicke, K; Mooers, A; Steel, M. (2021) Formal Links between Feature Diversity and Phylogenetic Diversity.Syst. Biol. 70: 480-490 Formal Links between Feature Diversity and Phylogenetic Diversity
Evolutionary distinctiveness; feature diversity; phylogenetic diversity; shapley value
The extent to which phylogenetic diversity (PD) captures feature diversity (FD) is a topical and controversial question in biodiversity conservation. In this short paper, we formalize this question and establish a precise mathematical condition for FD (based on discrete characters) to coincide with PD. In this way, we make explicit the two main reasons why the two diversity measures might disagree for given data; namely, the presence of certain patterns of feature evolution and loss, and using temporal branch lengths for PD in settings that may not be appropriate (e.g., due to rapid evolution of certain features over short periods of time). Our article also explores the relationship between the "Fair Proportion" index of PD and a simple index of FD (both of which correspond to Shapley values in cooperative game theory). In a second mathematical result, we show that the two indices can take identical values for any phylogenetic tree, provided the branch lengths in the tree are chosen appropriately. DOI PubMed
114. Biega, AM; Lamont, M; Mooers, A; Bowkett, AE; Martin, TE. (2019) Guiding the prioritization of the most endangered and evolutionary distinct birds for new zoo conservation programs.Zoo Biol. 38: 305-315 Guiding the prioritization of the most endangered and evolutionary distinct birds for new zoo conservation programs
Avian; captive breeding; ED; ex situ conservation; targets
Zoos have played a pivotal role in the successful reinforcement and reintroduction of species threatened with extinction, but prioritization is required in the face of increasing need and limited capacity. One means of prioritizing between species of equal threat status when establishing new breeding programs is the consideration of evolutionary distinctness (ED). More distinct species have fewer close relatives such that their extinction would result in a greater overall loss to the Tree of Life. Considering global ex situ holdings of birds (a group with a complete and well-detailed evolutionary tree), we investigate the representation of at-risk and highly evolutionarily distinct species in global zoo holdings. We identified a total of 2,236 bird species indicated by the Zoological Information Management System as being held in zoological institutions worldwide. As previously reported, imperiled species (defined as those possessing endangered or critically endangered threat status) in this database are less likely to be held in zoos than non-imperiled species. However, we find that species possessing ED scores within the top 10% of all bird species are more likely to be held in zoos than other species, possibly because they possess unique characteristics that have historically made them popular exhibits. To assist with the selection of high priority ED species for future zoo conservation programs, we provide a list of imperiled species currently not held in zoos, ranked by ED. This list highlights species representing particular priorities for ex situ conservation planners, and represents a practical tool for improving the conservation value of zoological collections. DOI PubMed
113. Cantalapiedra, JL; Aze, T; Cadotte, MW; Dalla Riva, GV; Huang, D; Mazel, F; Pennell, MW; Rios, M; Mooers, AO. (2019) Conserving evolutionary history does not result in greater diversity over geological time scales.Proc. R. Soc. B-Biol. Sci. 286 Conserving evolutionary history does not result in greater diversity over geological time scales
conservation; phylogenetic diversity; diversification; macroevolution
Alternative prioritization strategies have been proposed to safeguard biodiversity over macroevolutionary time scales. The first prioritizes the most distantly related species-maximizing phylogenetic diversity (PD)-in the hopes of capturing at least some lineages that will successfully diversify into the future. The second prioritizes lineages that are currently speciating, in the hopes that successful lineages will continue to generate species into the future. These contrasting schemes also map onto contrasting predictions about the role of slow diversifiers in the production of biodiversity over palaeontological time scales. We consider the performance of the two schemes across 10 dated species-level palaeo-phylogenetic trees ranging from Foraminifera to dinosaurs. We find that prioritizing PD for conservation generally led to fewer subsequent lineages, while prioritizing diversifiers led to modestly more subsequent diversity, compared with random sets of lineages. Importantly for conservation, the tree shape when decisions are made cannot predict which scheme will be most successful. These patterns are inconsistent with the notion that long-lived lineages are the source of new species. While there may be sound reasons for prioritizing PD for conservation, long-term species production might not be one of them. DOI PubMed
112. Lertzman-Lepofsky, G; Mooers, AO; Greenberg, DA. (2019) Ecological constraints associated with genome size across salamander lineages.Proc. R. Soc. B-Biol. Sci. 286 Ecological constraints associated with genome size across salamander lineages
c-value; Caudata; evolutionary constraint; transition rates; development time
Salamanders have some of the largest, and most variable, genome sizes among the vertebrates. Larger genomes have been associated with larger cell sizes, lower metabolic rates, and longer embryonic and larval durations in many different taxonomic groups. These life-history traits are often important for dictating fitness under different environmental conditions, suggesting that a species' genome site may have the potential to constrain its ecological distribution. We test how genome size varies with the ephemerality of larval habitat across the salamanders, predicting that species with larger genomes will be constrained to more permanent habitats that permit slower development, while species with smaller genomes will be more broadly distributed across the gradient of habitat ephemerality. We found that salamanders with larger genomes are almost exclusively associated with permanent aquatic habitats. In addition, the evolutionary transition rate between permanent and ephemeral larval habitats is much higher in salamander lineages with smaller genome sizes. These patterns suggest that genome size may act as an evolutionary constraint on the ecological habitats of salamanders, restricting those species with large genomes and slower development to habitats with permanent sources of water. DOI PubMed
110. Monroe, MJ; Butchart, SHM; Mooers, AO; Bokma, F. (2019) The dynamics underlying avian extinction trajectories forecast a wave of extinctions.Biol. Lett. 15 The dynamics underlying avian extinction trajectories forecast a wave of extinctions
biodiversity; birds; mass extinction; endangered species; conservation; population decline
Population decline is a process, yet estimates of current extinction rates often consider just the final step of that process by counting numbers of species lost in historical times. This neglects the increased extinction risk that affects a large proportion of species, and consequently underestimates the effective extinction rate. Here, we model observed trajectories through IUCN Red List extinction risk categories for all bird species globally over 28 years, and estimate an overall effective extinction rate of 2.17 x 10(-4)/species/year. This is six times higher than the rate of outright extinction since 1500, as a consequence of the large number of species whose status is deteriorating. We very conservatively estimate that global conservation efforts have reduced the effective extinction rate by 40%, but mostly through preventing critically endangered species from going extinct rather than by preventing species at low risk from moving into higher-risk categories. Our findings suggest that extinction risk in birds is accumulating much more than previously appreciated, but would be even greater without conservation efforts. DOI PubMed
108. Tucker, CM; Aze, T; Cadotte, MW; Cantalapiedra, JL; Chisholm, C; Diaz, S; Grenyer, R; Huang, DW; Mazel, F; Pearse, WD; Pennell, MW; Winter, M; Mooers, AO. (2019) Assessing the utility of conserving evolutionary history.Biol. Rev. 94: 1740-1760 Assessing the utility of conserving evolutionary history
phylogenetic diversity; conservation; prioritization; phenotypic diversity; ecosystem function; extinction; functional diversity; benefits to people
It is often claimed that conserving evolutionary history is more efficient than species-based approaches for capturing the attributes of biodiversity that benefit people. This claim underpins academic analyses and recommendations about the distribution and prioritization of species and areas for conservation, but evolutionary history is rarely considered in practical conservation activities. One impediment to implementation is that arguments related to the human-centric benefits of evolutionary history are often vague and the underlying mechanisms poorly explored. Herein we identify the arguments linking the prioritization of evolutionary history with benefits to people, and for each we explicate the purported mechanism, and evaluate its theoretical and empirical support. We find that, even after 25 years of academic research, the strength of evidence linking evolutionary history to human benefits is still fragile. Most - but not all - arguments rely on the assumption that evolutionary history is a useful surrogate for phenotypic diversity. This surrogacy relationship in turn underlies additional arguments, particularly that, by capturing more phenotypic diversity, evolutionary history will preserve greater ecosystem functioning, capture more of the natural variety that humans prefer, and allow the maintenance of future benefits to humans. A surrogate relationship between evolutionary history and phenotypic diversity appears reasonable given theoretical and empirical results, but the strength of this relationship varies greatly. To the extent that evolutionary history captures unmeasured phenotypic diversity, maximizing the representation of evolutionary history should capture variation in species characteristics that are otherwise unknown, supporting some of the existing arguments. However, there is great variation in the strength and availability of evidence for benefits associated with protecting phenotypic diversity. There are many studies finding positive biodiversity-ecosystem functioning relationships, but little work exists on the maintenance of future benefits or the degree to which humans prefer sets of species with high phenotypic diversity or evolutionary history. Although several arguments link the protection of evolutionary history directly with the reduction of extinction rates, and with the production of relatively greater future biodiversity via increased adaptation or diversification, there are few direct tests. Several of these putative benefits have mismatches between the relevant spatial scales for conservation actions and the spatial scales at which benefits to humans are realized. It will be important for future work to fill in some of these gaps through direct tests of the arguments we define here. DOI PubMed
107. Wilson, FM; Pappas, PA; Mooers, AO. (2019) The role of frequency of use in lexical change Evidence from Latin and Greek.Diachronica 36: 584-612 The role of frequency of use in lexical change Evidence from Latin and Greek
lexical change; frequency effects; language evolution; borrowing; Greek; Latin; Spanish
Based on the number of words per meaning across the Indo-European Swadesh list, Pagel et al. (2007) suggest that frequency of use is a general mechanism of linguistic evolution. We test this claim using within-language change. From the IDS (Key & Comrie 2015) we compiled a comparative word list of 1,147 cognate pairs for Classical Latin and Modern Spanish, and 1,231 cognate pairs for Classical and Modern Greek. We scored the amount of change for each cognate pair in the two language histories according to a novel 6-point scale reflecting increasing levels of change from regular sound change to external borrowing. We find a weak negative correlation between frequency of use and lexical change for both the Latin-Spanish and Classical-Modern Greek language developments, but post hoc tests reveal that low frequency of use of borrowed words drive these patterns, casting some doubt on frequency of use as a general mechanism of language change. DOI
106. Chaudhary, A; Mooers, AO. (2018) Terrestrial Vertebrate Biodiversity Loss under Future Global Land Use Change Scenarios.Sustainability 10 Terrestrial Vertebrate Biodiversity Loss under Future Global Land Use Change Scenarios
biodiversity; evolutionary history; future pathways; habitat loss; land use; species extinctions
Efficient forward-looking mitigation measures are needed to halt the global biodiversity decline. These require spatially explicit scenarios of expected changes in multiple indicators of biodiversity under future socio-economic and environmental conditions. Here, we link six future (2050 and 2100) global gridded maps (0.25 degrees x 0.25 degrees resolution) available from the land use harmonization (LUH) database, representing alternative concentration pathways (RCP) and shared socio-economic pathways (SSPs), with the countryside species-area relationship model to project the future land use change driven rates of species extinctions and phylogenetic diversity loss (in million years) for mammals, birds, and amphibians in each of the 804 terrestrial ecoregions and 176 countries and compare them with the current (1900-2015) and past (850-1900) rates of biodiversity loss. Future land-use changes are projected to commit an additional 209-818 endemic species and 1190-4402 million years of evolutionary history to extinction by 2100 depending upon the scenario. These estimates are driven by land use change only and would likely be higher once the direct effects of climate change on species are included. Among the three taxa, highest diversity loss is projected for amphibians. We found that the most aggressive climate mitigation scenario (RCP2.6 SSP-1), representing a world shifting towards a radically more sustainable path, including increasing crop yields, reduced meat production, and reduced tropical deforestation coupled with high trade, projects the lowest land use change driven global biodiversity loss. The results show that hotspots of future biodiversity loss differ depending upon the scenario, taxon, and metric considered. Future extinctions could potentially be reduced if habitat preservation is incorporated into national development plans, especially for biodiverse, low-income countries such as Indonesia, Madagascar, Tanzania, Philippines, and The Democratic Republic of Congo that are otherwise projected to suffer a high number of land use change driven extinctions under all scenarios. DOI
105. Chaudhary, A; Pourfaraj, V; Mooers, AO. (2018) Projecting global land use-driven evolutionary history loss.Divers. Distrib. 24: 158-167 Projecting global land use-driven evolutionary history loss
biodiversity; evolutionary history; habitat loss; land use; phylogenetic diversity; species extinctions
Aim: Recent studies have mapped the global hotspots hosting high phylogenetic diversity (PD), but not the regions where this diversity is under threat due to human land use. This is because, to date, it is not clear how much PD is lost as species of a given taxon go extinct. The aim of this study was to identify the global regions projected to suffer the highest PD loss due to human land use in the near future. Location: Global. Methods: We demonstrate a novel approach combining countryside species-area relationship, species-specific evolutionary distinctiveness (ED) scores and a newly derived strong linear relationship between the cumulative ED loss and PD loss through pruning simulations on global evolutionary trees of mammals, birds, and amphibians under random species loss, to project global land use-driven phylogenetic diversity loss in 804 terrestrial ecoregions and 175 countries. We also allocate the total projected PD loss to different land use types (agriculture, forestry, grazing or urbanization) in each region to pinpoint the major drivers. Results: For the three taxa combined, we project a total loss of 9,472 million years (MY) of evolutionary history due to all land uses in all countries: 1,541 MY of mammal PD is at stake, 3,336 MY of bird PD and 4,595 MY of amphibian PD. Agriculture is responsible for loss of 1,579 MY; pasture 1990 MY, forestry 5,381 and urbanization 522. Land use in Indonesia, Colombia, India, Papua New Guinea, Madagascar and Philippines is projected to cause the most loss of PD. Main conclusions: Through the integrated approach, we can now project PD loss associated with species extinctions under alternative land conversion scenarios in a region. Overall, the results on hotspots and land use drivers may inform individual nations in designing regional strategies to achieve the international biodiversity and sustainability targets. DOI
104. Greenberg, DA; Palen, WJ; Chan, KC; Jetz, W; Mooers, AO. (2018) Evolutionarily distinct amphibians are disproportionately lost from human-modified ecosystems.Ecology Letters 21 Evolutionarily distinct amphibians are disproportionately lost from human-modified ecosystems
diversification; extinction risk; forests; global change; grasslands; habitat loss; land conversion; phylogenetic diversity
Humans continue to alter terrestrial ecosystems, but our understanding of how biodiversity responds is still limited. Anthropogenic habitat conversion has been associated with the loss of evolutionarily distinct bird species at local scales, but whether this evolutionary pattern holds across other clades is unknown. We collate a global dataset on amphibian assemblages in intact forests and nearby human-modified sites to assess whether evolutionary history influences susceptibility to land conversion. We found that evolutionarily distinct amphibian species are disproportionately lost when forested habitats are converted to alternative land-uses. We tested the hypothesis that grassland-associated amphibian lineages have both higher diversification and are pre-adapted to human landscapes, but found only weak evidence supporting this. The loss of evolutionarily distinct amphibians with land conversion suggests that preserving remnant forests will be vital if we aim to preserve the amphibian tree of life in the face of mounting anthropogenic pressures. DOI PubMed
103. Lewthwaite, JMM; Angert, AL; Kembel, SW; Goring, SJ; Davies, TJ; Mooers, AO; Sperling, FAH; Vamosi, SM; Vamosi, JC; Kerr, JT. (2018) Canadian butterfly climate debt is significant and correlated with range size.Ecography 41 Canadian butterfly climate debt is significant and correlated with range size
climate debt; butterflies; global climate change; Canada; phylogenetics; life history; dispersal; range shifts; host plant
Climate change is causing rapid shifts in species' range limits, leading to poleward expansions and range losses toward the equator. However, 'climate debt', the gap between required and realized range shifts under changing climates, can accumulate when species are unable to track shifting conditions sufficiently rapidly to keep pace with climate changes. Currently, we do not know the rate at which species will keep pace via dispersal to track their climate envelopes, yet understanding potential differences in climate debt is central to estimating how climate change will influence extinction risk. Here, we use historical observations of 155 butterfly species found in Canada to construct climate-based environmental niche models for each species and then compare projections with observed modern distributions to quantify climate debts. This approach suggests that high levels of climate debt are accumulating within the vast majority of these species. Such failure to track changing climates may arise from some combination of interspecific interactions such as particular food availability for specialists, abiotic barriers such as mountain ranges, or species' intrinsic dispersal capacities. Our linear models relating climate debt to a variety of biological predictors suggest that the debts we documented are accumulating independently of dispersal ability, diet breadth, and phylogeny. A proxy for range size is the only significant predictor of climate debt, with species with narrower ranges accumulating more debt: this suggests that species with narrow ranges may be at risk from both a reduction of suitable habitat in their current range and the failure to colonize newly available habitat. Identifying the factors, whether intrinsic or imposed by local environmental conditions, that limit species' capacities to colonize areas beyond their historical limits is vital to conservation planning. DOI
102. Mazel, F; Pennell, MW; Cadotte, MW; Diaz, S; Dalla Riva, GV; Grenyer, R; Leprieur, F; Mooers, AO; Mouillot, D; Tucker, CM; Pearse, WD. (2018) Prioritizing phylogenetic diversity captures functional diversity unreliably.Nat. Commun. 9 Prioritizing phylogenetic diversity captures functional diversity unreliably
In the face of the biodiversity crisis, it is argued that we should prioritize species in order to capture high functional diversity (FD). Because species traits often reflect shared evolutionary history, many researchers have assumed that maximizing phylogenetic diversity (PD) should indirectly capture FD, a hypothesis that we name the "phylogenetic gambit". Here, we empirically test this gambit using data on ecologically relevant traits from >15,000 vertebrate species. Specifically, we estimate a measure of surrogacy of PD for FD. We find that maximizing PD results in an average gain of 18% of FD relative to random choice. However, this average gain obscures the fact that in over one-third of the comparisons, maximum PD sets contain less FD than randomly chosen sets of species. These results suggest that, while maximizing PD protection can help to protect FD, it represents a risky conservation strategy. DOI PubMed
99. Steel, M; Pourfaraj, V; Chaudhary, A; Mooers, A. (2018) Evolutionary isolation and phylogenetic diversity loss under random extinction events.Journal of Theoretical Biology 438: 151-155 Evolutionary isolation and phylogenetic diversity loss under random extinction events
Phylogenetic diversity; Fair proportion; Evolutionary distinctiveness; Birth-death models
The extinction of species at the present leads to the loss of 'phylogenetic diversity' (PD) from the evolutionary tree in which these species lie. Prior to extinction, the total PD present can be divided up among the species in various ways using measures of evolutionary isolation (such as 'fair proportion' and 'equal splits'). However, the loss of PD when certain combinations of species become extinct can be either larger or smaller than the cumulative loss of the isolation values associated with the extinct species. In this paper, we show that for trees generated under neutral evolutionary models, the loss of PD under a null model of random extinction at the present can be predicted from the loss of the cumulative isolation values, by applying a non-linear transformation that is independent of the tree. Moreover, the error in the prediction provably converges to zero as the size of the tree grows, with simulations showing good agreement even for moderate sized trees (n = 64). (C) 2017 Elsevier Ltd. All rights reserved. DOI
98. Stein, RW; Mull, CG; Kuhn, TS; Aschliman, NC; Davidson, LNK; Joy, JB; Smith, GJ; Dulvy, NK; Mooers, AO. (2018) Global priorities for conserving the evolutionary history of sharks, rays and chimaeras.Nat. Ecol. Evol. 2 Global priorities for conserving the evolutionary history of sharks, rays and chimaeras
In an era of accelerated biodiversity loss and limited conservation resources, systematic prioritization of species and places is essential. In terrestrial vertebrates, evolutionary distinctness has been used to identify species and locations that embody the greatest share of evolutionary history. We estimate evolutionary distinctness for a large marine vertebrate radiation on a dated taxon-complete tree for all 1,192 chondrichthyan fishes (sharks, rays and chimaeras) by augmenting a new 610-species molecular phylogeny using taxonomic constraints. Chondrichthyans are by far the most evolutionarily distinct of all major radiations of jawed vertebrates-the average species embodies 26 million years of unique evolutionary history. With this metric, we identify 21 countries with the highest richness, endemism and evolutionary distinctness of threatened species as targets for conservation prioritization. On average, threatened chondrichthyans are more evolutionarily distinct-further motivating improved conservation, fisheries management and trade regulation to avoid significant pruning of the chondrichthyan tree of life. DOI PubMed
97. Biega, A; Greenberg, DA; Mooers, AO; Jones, OR; Martin, TE. (2017) Global representation of threatened amphibians ex situ is bolstered by non-traditional institutions, but gaps remain.Animal Conservation 20: 113-119 Global representation of threatened amphibians ex situ is bolstered by non-traditional institutions, but gaps remain
amphibians; biogeography; ex situ conservation; extinction risk; species pairs; zoos; Amphibian Ark; conservation breeding; threat status
Ambitious global conservation targets have been set to manage increasing threats to amphibians. Ex situ institutions (broadly, zoos') are playing an expanding role in meeting these targets. Here, we examine the extent to which zoos house species representing the greatest overall conservation priority by testing how eight variables relating to extinction risk - International Union for the Conservation of Nature status, habitat specialization, obligate stream breeding, geographic range size, body size and island, high-altitude and tropical endemism - vary between amphibian species held in zoos and their close relatives not held in zoos. Based on 253 species found in zoos that could be confidently paired with close relatives not in zoos, and in contrast to reported patterns for birds and mammals, we find that amphibians currently held in zoos are equally as threatened as their close relatives not found in zoos. This result is entirely driven by the inclusion of data on species holdings from Amphibian Ark (AArk), an organization that helps to coordinate conservation activities in many non-traditional' institutions, as well as in traditional' commercial zoos. Such networks of small non-traditional institutions thus make meaningful contributions to ex situ conservation, and the establishment of other taxa-specific organizations modelled on AArk might be considered. That said, our results indicate that the ex situ network is still not prioritizing range-restricted habitat specialists, species that possess greater overall extinction risk in the near future. We strongly encourage zoos to continue increasing their holdings of amphibian species, but to pay greater attention to these species of particular conservation concern. DOI
96. Dembo, M; Mooers, A; Collard, M. (2017) "Rogue" Taxa and Hominin Phylogeny.Am. J. Phys. Anthropol. 162: 160-160 "Rogue" Taxa and Hominin Phylogeny
95. Greenberg, DA; Palen, WJ; Mooers, AO. (2017) Amphibian species traits, evolutionary history and environment predict Batrachochytrium dendrobatidis infection patterns, but not extinction risk.Evol. Appl. 10: 1130-1145 Amphibian species traits, evolutionary history and environment predict Batrachochytrium dendrobatidis infection patterns, but not extinction risk
amphibian; Batrachochytrium dendrobatidis; chytridiomycosis; extinction; phylogeny; resistance; tolerance; traits
The fungal pathogen Batrachochytrium dendrobatidis (B.dendrobatidis) has emerged as a major agent of amphibian extinction, requiring conservation intervention for many susceptible species. Identifying susceptible species is challenging, but many aspects of species biology are predicted to influence the evolution of host resistance, tolerance, or avoidance strategies towards disease. In turn, we may expect species exhibiting these distinct strategies to differ in their ability to survive epizootic disease outbreaks. Here, we test for phylogenetic and trait-based patterns of B.dendrobatidis infection risk and infection intensity among 302 amphibian species by compiling a global data set of B.dendrobatidis infection surveys across 95 sites. We then use best-fit models that associate traits, taxonomy and environment with B.dendrobatidis infection risk and intensity to predict host disease mitigation strategies (tolerance, resistance, avoidance) for 122 Neotropical amphibian species that experienced epizootic B.dendrobatidis outbreaks, and noted species persistence or extinction from these events. Aspects of amphibian species life history, habitat use and climatic niche were consistently linked to variation in B.dendrobatidis infection patterns across sites around the world. However, predicted B.dendrobatidis infection risk and intensity based on site environment and species traits did not reveal a consistent pattern between the predicted host disease mitigation strategy and extinction outcome. This suggests that either tolerant or resistant species may have no advantage in ameliorating disease during epizootic events, or that other factors drive the persistence of amphibian populations during chytridiomycosis outbreaks. These results suggest that using a trait-based approach may allow us to identify species with resistance or tolerance to endemic B.dendrobatidis infections, but that this approach may be insufficient to ultimately identify species at risk of extinction from epizootics. DOI
93. Mazel, F; Mooers, AO; Dalla Riva, GV; Pennell, MW. (2017) Conserving Phylogenetic Diversity Can Be a Poor Strategy for Conserving Functional Diversity.Syst. Biol. 66: 1019-1027 Conserving Phylogenetic Diversity Can Be a Poor Strategy for Conserving Functional Diversity
Conservation; evolutionary diversity; functional diversity; species prioritization; trait evolution
For decades, academic biologists have advocated for making conservation decisions in light of evolutionary history. Specifically, they suggest that policy makers should prioritize conserving phylogenetically diverse assemblages. The most prominent argument is that conserving phylogenetic diversity (PD) will also conserve diversity in traits and features (functional diversity [FD]), which may be valuable for a number of reasons. The claim that PD-maximized ("maxPD") sets of taxa will also have high FD is often taken at face value and in cases where researchers have actually tested it, they have done so by measuring the phylogenetic signal in ecologically important functional traits. The rationale is that if traits closely mirror phylogeny, then saving the maxPD set of taxa will tend to maximize FD and if traits do not have phylogenetic structure, then saving the maxPD set of taxa will be no better at capturing FD than criteria that ignore PD. Here, we suggest that measuring the phylogenetic signal in traits is uninformative for evaluating the effectiveness of using PD in conservation. We evolve traits under several different models and, for the first time, directly compare the FD of a set of taxa that maximize PD to the FD of a random set of the same size. Under many common models of trait evolution and tree shapes, conserving the maxPD set of taxa will conserve more FD than conserving a random set of the same size. However, this result cannot be generalized to other classes of models. We find that under biologically plausible scenarios, using PD to select species can actually lead to less FD compared with a random set. Critically, this can occur even when there is phylogenetic signal in the traits. Predicting exactly when we expect using PD to be a good strategy for conserving FD is challenging, as it depends on complex interactions between tree shape and the assumptions of the evolutionary model. Nonetheless, if our goal is to maintain trait diversity, the fact that conserving taxa based on PD will not reliably conserve at least as much FD as choosing randomly raises serious concerns about the general utility of PD in conservation. DOI
91. Tucker, CM; Cadotte, MW; Carvalho, SB; Davies, TJ; Ferrier, S; Fritz, SA; Grenyer, R; Helmus, MR; Jin, LS; Mooers, AO; Pavoine, S; Purschke, O; Redding, DW; Rosauer, DF; Winter, M; Mazel, F. (2017) A guide to phylogenetic metrics for conservation, community ecology and macroecology.Biol. Rev. 92: 698-715 A guide to phylogenetic metrics for conservation, community ecology and macroecology
biodiversity hotspots; biogeography; community assembly; conservation; diversity metrics; evolutionary history; phylogenetic diversity; prioritization; range size
The use of phylogenies in ecology is increasingly common and has broadened our understanding of biological diversity. Ecological sub-disciplines, particularly conservation, community ecology and macroecology, all recognize the value of evolutionary relationships but the resulting development of phylogenetic approaches has led to a proliferation of phylogenetic diversity metrics. The use of many metrics across the sub-disciplines hampers potential meta-analyses, syntheses, and generalizations of existing results. Further, there is no guide for selecting the appropriatemetric for a given question, and different metrics are frequently used to address similar questions. To improve the choice, application, and interpretation of phylo-diversity metrics, we organize existing metrics by expanding on a unifying framework for phylogenetic information. Generally, questions about phylogenetic relationships within or between assemblages tend to ask three types of question: how much; how different; or how regular? We show that these questions reflect three dimensions of a phylogenetic tree: richness, divergence, and regularity. We classify 70 existing phylo-diversity metrics based on their mathematical form within these three dimensions and identify 'anchor' representatives: for alpha-diversity metrics these are PD (Faith's phylogenetic diversity), MPD (mean pairwise distance), and VPD (variation of pairwise distances). By analysing mathematical formulae and using simulations, we use this framework to identify metrics that mix dimensions, and we provide a guide to choosing and using the most appropriate metrics. We show that metric choice requires connecting the research question with the correct dimension of the framework and that there are logical approaches to selecting and interpreting metrics. The guide outlined herein will help researchers navigate the current jungle of indices. DOI
90. Waldron, A; Miller, DC; Redding, D; Mooers, A; Kuhn, TS; Nibbelink, N; Roberts, JT; Tobias, JA; Gittleman, JL. (2017) Reductions in global biodiversity loss predicted from conservation spending.Nature 551: 364-+ Reductions in global biodiversity loss predicted from conservation spending
Halting global biodiversity loss is central to the Convention on Biological Diversity and United Nations Sustainable Development Goals(1,2), but success to date has been very limited(3-5). A critical determinant of success in achieving these goals is the financing that is committed to maintaining biodiversity(6-9); however, financing decisions are hindered by considerable uncertainty over the likely impact of any conservation investment(6-9). For greater effectiveness, we need an evidence-based model(10-12) that shows how conservation spending quantitatively reduces the rate of biodiversity loss. Here we demonstrate such a model, and empirically quantify how conservation investment between 1996 and 2008 reduced biodiversity loss in 109 countries (signatories to the Convention on Biological Diversity and Sustainable Development Goals), by a median average of 29% per country. We also show that biodiversity changes in signatory countries can be predicted with high accuracy, using a dual model that balances the effects of conservation investment against those of economic, agricultural and population growth (human development pressures)(13-18). Decision-makers can use this model to forecast the improvement that any proposed biodiversity budget would achieve under various scenarios of human development pressure, and then compare these forecasts to any chosen policy target. We find that the impact of spending decreases as human development pressures grow, which implies that funding may need to increase over time. The model offers a flexible tool for balancing the Sustainable Development Goals of human development and maintaining biodiversity, by predicting the dynamic changes in conservation finance that will be needed as human development proceeds. DOI
89. Dembo, M; Radovcic, D; Garvin, HM; Laird, ME; Schroeder, L; Scott, JE; Brophy, J; Ackermann, RR; Musiba, CM; de Ruiter, DJ; Mooers, AO; Collard, M. (2016) The evolutionary relationships and age of Homo naledi: An assessment using dated Bayesian phylogenetic methods.Journal of Human Evolution 97: 17-26 The evolutionary relationships and age of Homo naledi: An assessment using dated Bayesian phylogenetic methods
Dinaledi hominins; Bayesian phylogenetic analysis; Morphological clock; Genus Homo
Homo naledi is a recently discovered species of fossil hominin from South Africa. A considerable amount is already known about H. naledi but some important questions remain unanswered. Here we report a study that addressed two of them: "Where does H. naledi fit in the hominin evolutionary tree?" and "How old is it?" We used a large supermatrix of craniodental characters for both early and late hominin species and Bayesian phylogenetic techniques to carry out three analyses. First, we performed a dated Bayesian analysis to generate estimates of the evolutionary relationships of fossil hominins including H. naledi. Then we employed Bayes factor tests to compare the strength of support for hypotheses about the relationships of H. naledi suggested by the best-estimate trees. Lastly, we carried out a resampling analysis to assess the accuracy of the age estimate for H. naledi yielded by the dated Bayesian analysis. The analyses strongly supported the hypothesis that H. naledi forms a Glade with the other Homo species and Australopithecus sediba. The analyses were more ambiguous regarding the position of H. naledi within the (Homo, Au. sediba) Glade. A number of hypotheses were rejected, but several others were not. Based on the available craniodental data, Homo antecessor, Asian Homo erectus, Homo habilis, Homo floresiensis, Homo sapiens, and Au. sediba could all be the sister taxon of H. naledi. According to the dated Bayesian analysis, the most likely age for H. naledi is 912 ka. This age estimate was supported by the resampling analysis. Our findings have a number of implications. Most notably, they support the assignment of the new specimens to Homo, cast doubt on the claim that H. naledi is simply a variant of H. erectus, and suggest H. naledi is younger than has been previously proposed. (C) 2016 Elsevier Ltd. All rights reserved. DOI
88. Hurteau, LA; Mooers, AO; Reynolds, JD; Hocking, MD. (2016) Salmon nutrients are associated with the phylogenetic dispersion of riparian flowering-plant assemblages.Ecology 97: 450-460 Salmon nutrients are associated with the phylogenetic dispersion of riparian flowering-plant assemblages
angiosperms; community assembly; flowering plants; marine nutrient subsidy; mean nearest taxon distance; Oncorhynchus; phylogenetic community structure; salmon
A signature of nonrandom phylogenetic community structure has been interpreted as indicating community assembly processes. Significant clustering within the phylogenetic structure of a community can be caused by habitat filtering due to low nutrient availability. Nutrient limitation in temperate Pacific coastal rainforests can be alleviated to some extent by marine nutrient subsidies introduced by migrating salmon, which leave a quantitative signature on the makeup of plant communities near spawning streams. Thus, nutrient-mediated habitat filtering could be reduced by salmon nutrients. Here, we ask how salmon abundance affects the phylogenetic structure of riparian flowering plant assemblages across 50 watersheds in the Great Bear Rainforest of British Columbia, Canada. Based on a regional pool of 60 plant species, we found that assemblages become more phylogenetically dispersed and species poor adjacent to streams with higher salmon spawning density. In contrast, increased phylogenetic clumping and species richness was seen in sites with low salmon density, with steeper slopes, further from the stream edge, and within smaller watersheds. These observations are all consistent with abiotic habitat filtering and biotic competitive exclusion acting together across local and landscape-scale gradients in nutrient availability to structure assembly of riparian flowering plants. In this case, rich salmon nutrients appear to release riparian flowering-plant assemblages from the confines of a low-nutrient habitat filter that drives phylogenetic clustering. DOI
87. Jensen, EL; Mooers, AO; Caccone, A; Russello, MA. (2016) I-HEDGE: determining the optimum complementary sets of taxa for conservation using evolutionary isolation.PeerJ 4 I-HEDGE: determining the optimum complementary sets of taxa for conservation using evolutionary isolation
Conservation genetics; HEDGE; Mitochondrial control region; Shapley index; Noah's Ark problem
In the midst of the current biodiversity crisis, conservation efforts might profitably be directed rected towards ensuring that extinctions do not result m inordinate losses of evolutionary history. Numerous methods have been developed to evaluate the importance of species based on their contribution to total phylogenetic diversity on trees and networks, but existing methods fail to take complementarily into account, and thus cannot identify the best order or subset of taxa to protect: Here, we develop a novel iterative calculation of the heightened evolutionary distinctiveness arid globally endangered metric (I-HEDGE) that produces the optimal ranked list for conservation Prioritization taking into account complementarity and based on both phylogenetic diversity and extinction probability. We applied this metric to a phylogenetic network based on mitochondria) control region data from extant and recently extinct giant Galapagos tortoises, a highly endangered group of closely related species. We found that the restoration of two extinct species (a project currently underway) will contribute the greatest gain in phylogenetic diversity, and present an ordered list of rankings that is the optimum complementarity set for conservation prioritization. DOI
86. Dembo, M; Matzke, NJ; Mooers, AO; Collard, M. (2015) Bayesian analysis of a morphological supermatrix sheds light on controversial fossil hominin relationships.Proceedings of the Royal Society B-Biological Sciences 282: 133-141 Bayesian analysis of a morphological supermatrix sheds light on controversial fossil hominin relationships
human origins; phylogeny; Bayesian morphological analysis
The phylogenetic relationships of several hominin species remain controversial. Two methodological issues contribute to the uncertainty use of partial, inconsistent datasets and reliance on phylogenetic methods that are ill-suited to testing competing hypotheses. Here, we report a study designed to overcome these issues. We first compiled a supermatrix of craniodental characters for all widely accepted hominin species. We then took advantage of recently developed Bayesian methods for building trees of serially sampled tips to test among hypotheses that have been put forward in three of the most important current debates in hominin phylogenetics the relationship between Australopithecus sediba and Homo, the taxonomic status of the Dmanisi hominins, and the place of the so-called hobbit fossils from Flores, Indonesia, in the hominin tree. Based on our results, several published hypotheses can be statistically rejected. For example, the data do not support the claim that Dmanisi hominins and all other early Homo specimens represent a single species, nor that the hobbit fossils are the remains of small-bodied modern humans, one of whom had Down syndrome. More broadly, our study provides a new baseline dataset for future work on hominin phylogeny and illustrates the promise of Bayesian approaches for understanding hominin phylogenetic relationships. DOI
84. Faye, L; Matthey-Doret, R; Mooers, AO. (2015) Valuing species on the cheap.Animal Conservation 18: 313-314 Valuing species on the cheap
Read the Feature Paper: ; other Commentaries on this paper: ; and the Response from the authors: DOI
83. Redding, DW; Mooers, AO; Sekercioglu, CH; Collen, B. (2015) Global evolutionary isolation measures can capture key local conservation species in Nearctic and Neotropical bird communities.Philosophical Transactions of the Royal Society B-Biological Sciences 370 Global evolutionary isolation measures can capture key local conservation species in Nearctic and Neotropical bird communities
biogeography; community; extinction risk; phylogenetically distinct; phylogeny
Understanding how to prioritize among the most deserving imperilled species has been a focus of biodiversity science for the past three decades. Though global metrics that integrate evolutionary history and likelihood of loss have been successfully implemented, conservation is typically carried out at sub-global scales on communities of species rather than among members of complete taxonomic assemblages. Whether and how global measures map to a local scale has received little scrutiny. At a local scale, conservation-relevant assemblages of species are likely to be made up of relatively few species spread across a large phylogenetic tree, and as a consequence there are potentially relatively large amounts of evolutionary history at stake. We ask to what extent global metrics of evolutionary history are useful for conservation priority setting at the community level by evaluating the extent to which three global measures of evolutionary isolation (evolutionary distinctiveness (ED), average pairwise distance (APD) and the pendant edge or unique phylogenetic diversity (PD) contribution) capture community-level phylogenetic and trait diversity for a large sample of Neotropical and Nearctic bird communities. We find that prioritizing the most ED species globally safeguards more than twice the total PD of local communities on average, but that this does not translate into increased local trait diversity. By contrast, global APD is strongly related to the APD of those same species at the community level, and prioritizing these species also safeguards local PD and trait diversity. The next step for biologists is to understand the variation in the concordance of global and local level scores and what this means for conservation priorities: we need more directed research on the use of different measures of evolutionary isolation to determine which might best capture desirable aspects of biodiversity. DOI PubMed
82. Stein, RW; Brown, JW; Mooers, AO. (2015) A molecular genetic time scale demonstrates Cretaceous origins and multiple diversification rate shifts within the order Galliformes (Aves).Molecular Phylogenetics and Evolution 92: 155-164 A molecular genetic time scale demonstrates Cretaceous origins and multiple diversification rate shifts within the order Galliformes (Aves)
Galliformes; Bayesian; Phylogeny; Fossil calibration; Diversification analysis; Mass extinction
The phylogeny of Galliformes (landfowl) has been studied extensively; however, the associated chronologies have been criticized recently due to misplaced or misidentified fossil calibrations. As a consequence, it is unclear whether any crown-group lineages arose in the Cretaceous and survived the Cretaceous-Paleogene (K-Pg; 65.5 Ma) mass extinction. Using Bayesian phylogenetic inference on an alignment spanning 14,539 bp of mitochondrial and nuclear DNA sequence data, four fossil calibrations, and a combination of uncorrelated lognormally distributed relaxed-clock and strict-clock models, we inferred a time-calibrated molecular phylogeny for 225 of the 291 extant Galliform taxa. These analyses suggest that crown Galliformes diversified in the Cretaceous and that three-stem lineages survived the K-Pg mass extinction. Ideally, characterizing the tempo and mode of diversification involves a taxonomically complete phylogenetic hypothesis. We used simple constraint structures to incorporate 66 data-deficient taxa and inferred the first taxon-complete phylogenetic hypothesis for the Galliformes. Diversification analyses conducted on 10,000 timetrees sampled from the posterior distribution of candidate trees show that the evolutionary history of the Galliformes is best explained by a rate-shift model including 1-3 clade-specific increases in diversification rate. We further show that the tempo and mode of diversification in the Galliformes conforms to a three-pulse model, with three-stem lineages arising in the Cretaceous and inter and intrafamilial diversification occurring after the K-Pg mass extinction, in the Paleocene-Eocene (65.5-33.9 Ma) or in association with the Eocene-Oligocene transition (33.9 Ma). (C) 2015 Elsevier Inc. All rights reserved. DOI
81. Volkmann, LA; Statham, MJ; Mooers, AO; Sacks, BN. (2015) Genetic distinctiveness of red foxes in the Intermountain West as revealed through expanded mitochondrial sequencing.Journal of Mammalogy 96: 297-307 Genetic distinctiveness of red foxes in the Intermountain West as revealed through expanded mitochondrial sequencing
Great Basin; mitochondrial DNA; phylogeography; population genetics; red fox; Vulpes vulpes
Western North America contains a mosaic of indigenous and introduced red fox (Vulpes vulpes) populations. Historically, native red foxes occurred in subalpine zones of the Cascade, Rocky, and Sierra Nevada mountain ranges, and in the desert-like Sacramento Valley of California. The origins of red foxes observed in the Intermountain West since the early 1900s are unclear, potentially representing native population relicts from the last ice age, dispersers from adjacent mountain populations, or early fur-farm escapees. These foxes carry a native 696-bp mitochondrial haplotype (A-19), which was also the most basal and widespread among western populations and thus equally consistent with ancient and contemporary origins. Here, to increase resolution, we sequenced an additional 3,308 bp (totaling 4,004 bp) of the mitochondrial genome corresponding to A-19 and related haplotypes (O-24 and D-19) from historical and modern samples collected throughout western North America. The expanded sequences revealed previously undocumented haplotype diversity, including another novel mutation associated with the D-19 matriline endemic to the Sacramento Valley, confirming its ancient divergence. We observed 6 A-19 variants falling into 2 divergent subclades. Although no A-19 variants were unique to the Intermountain West, the 2 dominant ones were rare elsewhere, and an analysis of molecular variance supported the distinctiveness of this population. Our findings suggest this population was either an ancient relict or derived from a small founder group from a neighboring mountain range. Additional sampling and high-density nuclear genomic markers can further clarify origins of these animals, including potential nonnative introgression. DOI
80. Cantalapiedra, JL; FitzJohn, RG; Kuhn, TS; Fernandez, MH; DeMiguel, D; Azanza, B; Morales, J; Mooers, AO. (2014) Dietary innovations spurred the diversification of ruminants during the Caenozoic.Proceedings of the Royal Society B-Biological Sciences 281 Dietary innovations spurred the diversification of ruminants during the Caenozoic
ruminants; Artiodactyla; diet evolution; diversification; palaeoclimate; phylogenetics
Global climate shifts and ecological flexibility are two major factors that may affect rates of speciation and extinction across clades. Here, we connect past climate to changes in diet and diversification dynamics of ruminant mammals. Using novel versions of Multi-State Speciation and Extinction models, we explore the most likely scenarios for evolutionary transitions among diets in this clade and ask whether ruminant lineages with different feeding styles (browsing, grazing and mixed feeding) underwent differential rates of diversification concomitant with global temperature change. The best model of trait change had transitions from browsers to grazers via mixed feeding, with appreciable rates of transition to and from grazing and mixed feeding. Diversification rates in mixed-feeder and grazer lineages tracked the palaeotemperature curve, exhibiting higher rates during the Miocene thermal maxima. The origination of facultative mixed diet and grazing states may have triggered two adaptive radiations-one during the Oligocene-Miocene transition and the other during Middle-to-Late Miocene. Our estimate of mixed diets for basal lineages of both bovids and cervids is congruent with fossil evidence, while the reconstruction of browser ancestors for some impoverished clades-Giraffidae and Tragulidae-is not. Our results offer model-based neontological support to previous palaeontological findings and fossil-based hypothesis highlighting the importance of dietary innovations-especially mixed feeding-in the success of ruminants during the Neogene. DOI
78. Elliot, MG; Mooers, AO. (2014) Inferring ancestral states without assuming neutrality or gradualism using a stable model of continuous character evolution.BMC Evolutionary Biology 14 Inferring ancestral states without assuming neutrality or gradualism using a stable model of continuous character evolution
Comparative methods; Ancestral state reconstruction; Evolutionary models
Background: The value of a continuous character evolving on a phylogenetic tree is commonly modelled as the location of a particle moving under one-dimensional Brownian motion with constant rate. The Brownian motion model is best suited to characters evolving under neutral drift or tracking an optimum that drifts neutrally. We present a generalization of the Brownian motion model which relaxes assumptions of neutrality and gradualism by considering increments to evolving characters to be drawn from a heavy-tailed stable distribution (of which the normal distribution is a specialized form). Results: We describe Markov chain Monte Carlo methods for fitting the model to biological data paying special attention to ancestral state reconstruction, and study the performance of the model in comparison with a selection of existing comparative methods, using both simulated data and a database of body mass in 1,679 mammalian species. We discuss hypothesis testing and model selection. The stable model outperforms Brownian and Ornstein-Uhlenbeck approaches under simulations in which traits evolve with occasional large "jumps" in their value, but does not perform markedly worse for traits evolving under a truly Brownian process. Conclusions: The stable model is well suited to a stochastic process with a volatile rate of change in which biological characters undergo a mixture of neutral drift and occasional evolutionary events of large magnitude. DOI PubMed
76. Jackson, G; Mooers, AO; Dubman, E; Hutchen, J; Collard, M. (2014) Basal metabolic rate and maternal energetic investment durations in mammals.BMC Evolutionary Biology 14 Basal metabolic rate and maternal energetic investment durations in mammals
Background: The Metabolic Theory of Ecology (MTE) predicts that gestation duration, lactation duration, and their sum, total development time, are constrained by mass-specific basal metabolic rate such that they should scale with body mass with an exponent of 0.25. However, tests of the MTE's predictions have yielded mixed results. In an effort to resolve this uncertainty, we used phylogenetically-controlled regression to investigate the allometries of gestation duration, lactation duration, and total development time in four well-studied mammalian orders, Artiodactyla, Carnivora, Primates, and Rodentia. Results: The results we obtained are not consistent with the predictions of the MTE. Gestation duration scaling exponents are below 0.25 in all four orders. The scaling exponent for lactation duration is below 0.25 in Carnivora and Rodentia, indistinguishable from 0.25 in Artiodactyls, and steeper than 0.25 in Primates. Total development time scales with body mass as predicted by the MTE in Primates, but not in artiodactyls, carnivores, and rodents. In the latter three orders, the exponent is 0.15. Conclusions: Together, these results indicate that the influence of basal metabolic rate on mammalian maternal investment durations must be more complicated than the MTE envisages, and that other factors must play an important role. Future research needs to allow for the possibility that different factors drive gestation duration and lactation duration, and that the drivers of the two durations may differ among orders. DOI PubMed
75. Jetz, W; Thomas, GH; Joy, JB; Redding, DW; Hartmann, K; Mooers, AO. (2014) Global Distribution and Conservation of Evolutionary Distinctness in Birds.Current Biology 24: 919-930 Global Distribution and Conservation of Evolutionary Distinctness in Birds
Background: Integrated, efficient, and global prioritization approaches are necessary to manage the ongoing loss of species and their associated function. "Evolutionary distinctness" measures a species' contribution to the total evolutionary history of its clade and is expected to capture uniquely divergent genomes and functions. Here we demonstrate how such a metric identifies species and regions of particular value for safeguarding evolutionary diversity. Results: Among the world's 9,993 recognized bird species, evolutionary distinctness is very heterogeneously distributed on the phylogenetic tree and varies little with range size or threat level. Species representing the most evolutionary history over the smallest area (those with greatest "evolutionary distinctness rarity") as well as some of the most imperiled distinct species are often concentrated outside the species-rich regions and countries, suggesting they may not be well captured by current conservation planning. We perform global cross-species and spatial analyses and generate minimum conservation sets to assess the benefits of the presented species-level metrics. We find that prioritizing imperiled species by their evolutionary distinctness and geographic rarity is a surprisingly effective and spatially economical way to maintain the total evolutionary information encompassing the world's birds. We identify potential conservation gaps in relation to the existing reserve network that in particular highlight islands as effective priority areas. Conclusions: The presented distinctness metrics are effective yet easily communicable and versatile tools to assist objective global conservation decision making. Given that most species will remain ecologically understudied, combining growing phylogenetic and spatial data may be an efficient way to retain vital aspects of biodiversity. DOI
74. Martin, TE; Lurbiecki, H; Joy, JB; Mooers, AO. (2014) Mammal and bird species held in zoos are less endemic and less threatened than their close relatives not held in zoos.Animal Conservation 17: 89-96 Mammal and bird species held in zoos are less endemic and less threatened than their close relatives not held in zoos
birds; ex situ conservation; zoos; mammals; biogeography; extinction
Zoos and related institutions make important contributions to the conservation of global biodiversity. However, resource constraints have led to certain faunal groupings being better represented in ex situ breeding programmes than others. Some broad patterns of faunal representation in zoos have been identified, although finer-scale differences within taxonomical families remain poorly understood, as do the influence of many geographical and ecological factors. Using a novel paired-species comparison approach, we investigate for the first time how seven of these variables can influence the current representation of mammal and bird species in zoos. Using data from 550 high-quality zoos worldwide, we identified 165 mammal and 228 bird species held in zoos that could be paired with clearly identifiable closest relatives not currently held in zoos. These matched pairs were then compared for threat level, zoogeographical distribution (including global hotspot endemism), spatial range, body mass, island habitat and altitudinal range. Results indicate that mammal and bird species in zoos are, on average, not only larger than their close relatives not held in zoos, but also possess larger spatial ranges, are less likely to be endemic and are distributed in lower-risk geographical regions. Importantly, they also tend to be less, rather than more, threatened with extinction. Multivariate models confirm that many of these correlated predictors act independently. We suggest that key mechanisms which can increase the inherent conservation risk of mammal and bird species can also act as barriers to their representation in zoos, and that this may contribute to a disparity between where ex situ resources are spent and where they are most needed. DOI
73. Martin, TE; Lurbiecki, H; Mooers, AO. (2014) The economic geography of ex situ conservation.Animal Conservation 17: 104-105 The economic geography of ex situ conservation
Read the Feature Paper: Commentaries on this Feature Paper: ; DOI
71. Redding, DW; Mazel, F; Mooers, AO. (2014) Measuring Evolutionary Isolation for Conservation.PLOS One 9 Measuring Evolutionary Isolation for Conservation
Conservation planning needs to account for limited resources when choosing those species on which to focus attention and resources. Currently, funding is biased to small sections of the tree of life, such as raptors and carnivores. One new approach for increasing the diversity of species under consideration considers how many close relatives a species has in its evolutionary tree. At least eleven different ways to measure this characteristic on phylogenies for the purposes of setting species-specific priorities for conservation have been proposed. We find that there is much redundancy within the current set, with three pairs of metrics being essentially identical. Non-redundant metrics represent different trade-offs between the unique evolutionary history represented by a species verses its average distance to all other species. Depending on which metric is used, species priority lists can differ as much as 85% for the top 100 species. We call for some consensus on the theory behind these metrics and suggest that all future developments are compared to the current published set, and offer scripts to aid such comparisons. DOI
70. Stephenson, S; Mooers, A; Attaran, A. (2014) Does Size Matter? The ICRW and the Inclusion of Small Cetaceans.Transnational Environmental Law 3: 241-263 Does Size Matter? The ICRW and the Inclusion of Small Cetaceans
International Environmental Law; Small Cetaceans; Whaling; Biodiversity; International Court of Justice
The competency debate over small cetacean regulation at the International Whaling Commission (IWC) is legal in nature, yet has been in a political stalemate for years. In this article we argue that the IWC has the competence to regulate small cetaceans and that the commercial whaling of 'small cetaceans' is a violation of the moratorium on commercial whaling. We present hybrid legal and scientific arguments and counter-arguments for the treaty interpretation of the International Convention for the Regulation of Whaling and, given recent precedent, advocate that the International Court of Justice be called upon to resolve this matter. DOI
68. Vamosi, JC; Moray, CM; Garcha, NK; Chamberlain, SA; Mooers, AO. (2014) Pollinators visit related plant species across 29 plant-pollinator networks.Ecology and Evolution 4: 2303-2315 Pollinators visit related plant species across 29 plant-pollinator networks
Competition; linkage rules; phylogenetic community ecology; phylogenetic signal; plant-pollinator networks
Understanding the evolution of specialization in host plant use by pollinators is often complicated by variability in the ecological context of specialization. Flowering communities offer their pollinators varying numbers and proportions of floral resources, and the uniformity observed in these floral resources is, to some degree, due to shared ancestry. Here, we find that pollinators visit related plant species more so than expected by chance throughout 29 plant-pollinator networks of varying sizes, with "clade specialization" increasing with community size. As predicted, less versatile pollinators showed more clade specialization overall. We then asked whether this clade specialization varied with the ratio of pollinator species to plant species such that pollinators were changing their behavior when there was increased competition (and presumably a forced narrowing of the realized niche) by examining pollinators that were present in at least three of the networks. Surprisingly, we found little evidence that variation in clade specialization is caused by pollinator species changing their behavior in different community contexts, suggesting that clade specialization is observed when pollinators are either restricted in their floral choices due to morphological constraints or innate preferences. The resulting pollinator sharing between closely related plant species could result in selection for greater pollinator specialization. DOI PubMed
67. Volkmann, L; Martyn, I; Moulton, V; Spillner, A; Mooers, AO. (2014) Prioritizing Populations for Conservation Using Phylogenetic Networks.PLOS One 9 Prioritizing Populations for Conservation Using Phylogenetic Networks
In the face of inevitable future losses to biodiversity, ranking species by conservation priority seems more than prudent. Setting conservation priorities within species (i.e., at the population level) may be critical as species ranges become fragmented and connectivity declines. However, existing approaches to prioritization (e. g., scoring organisms by their expected genetic contribution) are based on phylogenetic trees, which may be poor representations of differentiation below the species level. In this paper we extend evolutionary isolation indices used in conservation planning from phylogenetic trees to phylogenetic networks. Such networks better represent population differentiation, and our extension allows populations to be ranked in order of their expected contribution to the set. We illustrate the approach using data from two imperiled species: the spotted owl Strix occidentalis in North America and the mountain pygmy-possum Burramys parvus in Australia. Using previously published mitochondrial and microsatellite data, we construct phylogenetic networks and score each population by its relative genetic distinctiveness. In both cases, our phylogenetic networks capture the geographic structure of each species: geographically peripheral populations harbor less-redundant genetic information, increasing their conservation rankings. We note that our approach can be used with all conservation-relevant distances (e. g., those based on whole-genome, ecological, or adaptive variation) and suggest it be added to the assortment of tools available to wildlife managers for allocating effort among threatened populations. DOI PubMed
66. Gudde, RM; Joy, JB; Mooers, AO. (2013) Imperilled phylogenetic endemism of Malagasy lemuriformes.Diversity and Distributions 19: 664-675 Imperilled phylogenetic endemism of Malagasy lemuriformes
IUCN RED LIST; CONSERVATION PRIORITIES; EVOLUTIONARY HISTORY; SPECIES RICHNESS; BIODIVERSITY CONSERVATION; MADAGASCAR LEMURS; MIXED MODELS; DIVERSITY; EXTINCTION; HOTSPOTS
Aim To highlight where in Madagascar the phylogenetically and spatially rare lemur species at risk of extinction are concentrated. Location Madagascar. Methods Phylogenetic endemism (PE) is a combined measure for apportioning a phylogenetic tree across a landscape used to identify those geographical locations that contain spatially rare phylogenetic diversity (Rosauer etal., 2009). We present a simple extension (imperilled phylogenetic endemism) that scales this phylogenetic diversity by the probability of its loss to extinction. We apply these measures to a composite phylogeny of all confirmed Malagasy lemuriform species using International Union for Conservation of Nature (IUCN) extent of occurrence and threat status data. Results We find that, because nonimperilled species are scattered about the lemuriform tree, interior branches of the tree are still quite secure: this also means that areas of high phylogenetic endemism for Madagascar lemuriformes are often the same areas as those of high imperilled PE (IPE), as both are heavily weighted by branches nearer the tips. However, although the North of Madagascar holds the largest amount of spatially rare evolutionary history using both PE and IPE, there are additional pockets of imperilled history in the south and west. Main Conclusions Correlations of endemism and threat status with phylogenetic isolation are modest across lemurs and so are not substitutable conservation values. They might best be integrated on the landscape using IPE. As illustrated here, IPE successfully highlights areas containing species which are at once threatened with extinction and that are phylogenetically and spatially rare. DOI
64. Thomas, GH; Hartmann, K; Jetz, W; Joy, JB; Mimoto, A; Mooers, AO. (2013) PASTIS: an R package to facilitate phylogenetic assembly with soft taxonomic inferences.Methods in Ecology and Evolution 4: 1011-1017 PASTIS: an R package to facilitate phylogenetic assembly with soft taxonomic inferences
MOLECULAR PHYLOGENIES; DIVERSIFICATION; BIRDS; DIVERSITY; MAMMALS; SPACE; TRAIT
1. Phylogenetic trees that include all member lineages are necessary for many questions in macroevolution, biogeography and conservation. Currently, producing such trees when genetic data or phenotypic characters for some tips are missing generally involves assigning missing species to the root of their most exclusive clade, essentially grafting them onto existing and static topologies as polytomies. 2. We describe an R package, PASTIS', that enables a two-stage Bayesian method using MrBayes version 3.2 (or higher) to incorporate lineages lacking genetic data at the tree inference stage. The inputs include a consensus topology, a set of taxonomic statements (e.g. placing species in genera and aligning some genera with each other or placing subspecies within species) and user-defined priors on edge lengths and topologies. PASTIS produces input files for execution in MrBayes that will produce a posterior distribution of complete ultrametric trees that captures uncertainty under a homogeneous birth-death prior model of diversification and placement constraints. If the age distribution of a focal node is known (e.g. from fossils), the ultrametric tree distribution can be converted to a set of dated trees. We also provide functions to visualize the placement of missing taxa in the posterior distribution. 3. The PASTIS approach is not limited to the level of species and could equally be applied to higher or lower levels of organization (e.g. accounting for all recognized subspecies or populations within a species) given an appropriate choice of priors on branching times. DOI
63. Barnosky, AD; Hadly, EA; Bascompte, J; Berlow, EL; Brown, JH; Fortelius, M; Getz, WM; Harte, J; Hastings, A; Marquet, PA; Martinez, ND; Mooers, A; Roopnarine, P; Vermeij, G; Williams, JW; Gillespie, R; Kitzes, J; Marshall, C; Matzke, N; Mindell, DP; Revilla, E; Smith, AB. (2012) Approaching a state shift in Earth's biosphere.Nature 486: 52-58 Approaching a state shift in Earth's biosphere
Localized ecological systems are known to shift abruptly and irreversibly from one state to another when they are forced across critical thresholds. Here we review evidence that the global ecosystem as a whole can react in the same way and is approaching a planetary-scale critical transition as a result of human influence. The plausibility of a planetary-scale 'tipping point' highlights the need to improve biological forecasting by detecting early warning signs of critical transitions on global as well as local scales, and by detecting feedbacks that promote such transitions. It is also necessary to address root causes of how humans are forcing biological changes. DOI
62. Jetz, W; Thomas, GH; Joy, JB; Hartmann, K; Mooers, AO. (2012) The global diversity of birds in space and time.Nature 491: 444-448 The global diversity of birds in space and time
Current global patterns of biodiversity result from processes that operate over both space and time and thus require an integrated macroecological and macroevolutionary perspective(1-4). Molecular time trees have advanced our understanding of the tempo and mode of diversification(5-7) and have identified remarkable adaptive radiations across the tree of life(8-10). However, incomplete joint phylogenetic and geographic sampling has limited broad-scale inference. Thus, the relative prevalence of rapid radiations and the importance of their geographic settings in shaping global biodiversity patterns remain unclear. Here we present, analyse and map the first complete dated phylogeny of all 9,993 extant species of birds, a widely studied group showing many unique adaptations. We find that birds have undergone a strong increase in diversification rate from about 50 million years ago to the near present. This acceleration is due to a number of significant rate increases, both within songbirds and within other young and mostly temperate radiations including the waterfowl, gulls and woodpeckers. Importantly, species characterized with very high past diversification rates are interspersed throughout the avian tree and across geographic space. Geographically, the major differences in diversification rates are hemispheric rather than latitudinal, with bird assemblages in Asia, North America and southern South America containing a disproportionate number of species from recent rapid radiations. The contribution of rapidly radiating lineages to both temporal diversification dynamics and spatial distributions of species diversity illustrates the benefits of an inclusive geographical and taxonomical perspective. Overall, whereas constituent clades may exhibit slowdowns(10,11), the adaptive zone into which modern birds have diversified since the Cretaceous may still offer opportunities for diversification. DOI
61. Martyn, I; Kuhn, TS; Mooers, AO; Moulton, V; Spillner, A. (2012) Computing evolutionary distinctiveness indices in large scale analysis.Algorithms For Molecular Biology 7 Computing evolutionary distinctiveness indices in large scale analysis
PHYLOGENETIC DIVERSITY; CONSERVATION; EXTINCTION; PROBABILITIES
We present optimal linear time algorithms for computing the Shapley values and 'heightened evolutionary distinctiveness' (HED) scores for the set of taxa in a phylogenetic tree. We demonstrate the efficiency of these new algorithms by applying them to a set of 10,000 reasonable 5139-species mammal trees. This is the first time these indices have been computed on such a large taxon and we contrast our finding with an ad-hoc index for mammals, fair proportion (FP), used by the Zoological Society of London's EDGE programme. Our empirical results follow expectations. In particular, the Shapley values are very strongly correlated with the FP scores, but provide a higher weight to the few monotremes that comprise the sister to all other mammals. We also find that the HED score, which measures a species' unique contribution to future subsets as function of the probability that close relatives will go extinct, is very sensitive to the estimated probabilities. When they are low, HED scores are less than FP scores, and approach the simple measure of a species' age. Deviations (like the Solendon genus of the West Indies) occur when sister species are both at high risk of extinction and their clade roots deep in the tree. Conversely, when endangered species have higher probabilities of being lost, HED scores can be greater than FP scores and species like the African elephant Loxondonta africana, the two solendons and the thumbless bat Furipterus horrens can move up the rankings. We suggest that conservation attention be applied to such species that carry genetic responsibility for imperiled close relatives. We also briefly discuss extensions of Shapley values and HED scores that are possible with the algorithms presented here. DOI
60.Mooers, A; Gascuel, O; Stadler, T; Li, HY; Steel, M. (2012) Branch Lengths on Birth-Death Trees and the Expected Loss of Phylogenetic Diversity.Systematic Biology 61: 195-203 Branch Lengths on Birth-Death Trees and the Expected Loss of Phylogenetic Diversity
EVOLUTIONARY HISTORY; DIVERSIFICATION RATES; NONRANDOM EXTINCTION; SPECIATION RATES; NEUTRAL MODELS; PATTERNS; SHAPE; TIME
Diversification is nested, and early models suggested this could lead to a great deal of evolutionary redundancy in the Tree of Life. This result is based on a particular set of branch lengths produced by the common coalescent, where pendant branches leading to tips can be very short compared with branches deeper in the tree. Here, we analyze alternative and more realistic Yule and birth-death models. We show how censoring at the present both makes average branches one half what we might expect and makes pendant and interior branches roughly equal in length. Although dependent on whether we condition on the size of the tree, its age, or both, these results hold both for the Yule model and for birth-death models with moderate extinction. Importantly, the rough equivalency in interior and exterior branch lengths means that the loss of evolutionary history with loss of species can be roughly linear. Under these models, the Tree of Life may offer limited redundancy in the face of ongoing species loss. DOI PubMed
59. Bokal, D; DeVos, M; Klavzar, S; Mimoto, A; Mooers, AO. (2011) Computing quadratic entropy in evolutionary trees.Computers & Mathematics With Applications 62: 3821-3828 Computing quadratic entropy in evolutionary trees
Evolutionary tree; Phylogenetic tree; Quadratic entropy; Originality; Distinctness; Wiener index
We note here that quadratic entropy, a measure of biological diversity introduced by C.R. Rao, is a variant of the weighted Wiener index, a graph invariant intensively studied in mathematical chemistry. This fact allows us to deduce some efficient algorithms for computing the quadratic entropy in the case of given tip weights, which may be useful for community biodiversity measures. Furthermore, on ultrametric phylogenetic trees, the maximum of quadratic entropy is a measure of pairwise evolutionary distinctness in conservation biology, introduced by S. Pavoine. We present an algorithm that maximizes this quantity in linear time, offering a significant improvement over the currently used quadratic programming approaches. (C) 2011 Elsevier Ltd. All rights reserved. DOI
58. Kuhn, TS; Mooers, AO; Thomas, GH. (2011) A simple polytomy resolver for dated phylogenies.Methods in Ecology and Evolution 2: 427-436 A simple polytomy resolver for dated phylogenies
MOLECULAR PHYLOGENIES; SPECIATION; EXTINCTION; EVOLUTION; DIVERSIFICATION; RESOLUTION; SUPERTREE; MAMMALS; RATES
1. Unresolved nodes in phylogenetic trees (polytomies) have long been recognized for their influences on specific phylogenetic metrics such as topological imbalance measures, diversification rate analysis and measures of phylogenetic diversity. However, no rigorously tested, biologically appropriate method has been proposed for overcoming the effects of this phylogenetic uncertainty. 2. Here, we present a simple approach to polytomy resolution, using biologically relevant models of diversification. Using the powerful and highly customizable phylogenetic inference and analysis software beast and R, we present a semi-automated 'polytomy resolver' capable of providing a distribution of tree topologies and branch lengths under specified biological models. 3. Utilizing both simulated and empirical data sets, we explore the effects and characteristics of this approach on two widely used phylogenetic tree statistics, Pybus' gamma (gamma) and Colless' normalized tree imbalance (I-c). Using simulated pure birth trees, we find no evidence of bias in either estimate using our resolver. Applying our approach to a recently published Cetacean phylogeny, we observed the expected small positive bias in gamma and decrease in I-c. 4. We further test the effect of polytomy resolution on diversification rate analysis using the Cetacean phylogeny. We demonstrate that using a birth-death model to resolve the Cetacean tree with 20%, 40% and 60% of random nodes collapsed to polytomies gave qualitatively similar patterns regarding the tempo and mode of diversification as the same analyses on the original, fully resolved phylogeny. 5. Finally, we applied the birth-death polytomy resolution approach to a large (>5000 tips), but unresolved, supertree of extant mammals. We report a distribution of fully resolved model-based trees, which should be useful for many future analysis of the mammalian supertree. DOI
57. Pappas, Panayiotis A.; Mooers, Arne O. (2011) Phylogenetic Methods in Historical Linguistics: Greek as a Case Study.Journal of Greek Linguistics, Volume 11, Number 2, 2011 , pp. 198-220(23) 11: 198-220 Phylogenetic Methods in Historical Linguistics: Greek as a Case Study
We review and assess the different ways in which research in evolutionary-theory-inspired biology has influenced research in historical linguistics, and then focus on an evolutionary-theory inspired claim for language change made by Pagel et al. (2007). They report that the more Swadesh-list lexemes are used, the less likely they are to change across 87 Indo-European languages, and posit that frequency-of-use of a lexical item is a separate and general mechanism of language change. We test a corollary of this conclusion, namely that current frequency-of-use should predict the amount of change within individual languages through time. We devise a scale of lexical change that recognizes sound change, analogical change and lexical replacement and apply it to cognate pairs on the Swadesh list between Homeric and Modern Greek. Current frequency-of-use only weakly predicts the amount of change within the history of Greek, but amount of change does predict the number of forms across Indo-European. Given that current frequency-of-use and past frequency-of-use may be only weakly correlated for many Swadesh-list lexemes, and given previous research that shows that frequency-of-use can both hinder and facilitate lexical change, we conclude that it is premature to claim that a new mechanism of language change has been discovered. However, we call for more in-depth comparative study of general mechanisms of language change, including further tests of the frequency-of-use hypothesis.
DOI
56. Parhar, RK; Mooers, AO. (2011) Phylogenetically Clustered Extinction Risks Do Not Substantially Prune the Tree of Life.PLOS One 6 Phylogenetically Clustered Extinction Risks Do Not Substantially Prune the Tree of Life
EVOLUTIONARY HISTORY; BIODIVERSITY CONSERVATION; MOLECULAR PHYLOGENIES; NONRANDOM EXTINCTION; MAMMALIAN DIVERSITY; PATTERNS; DIVERSIFICATION; SPECIATION; MODELS; SIGNAL
Anthropogenic activities have increased the rate of biological extinction many-fold. Recent empirical studies suggest that projected extinction may lead to extensive loss to the Tree of Life, much more than if extinction were random. One suggested cause is that extinction risk is heritable (phylogenetically patterned), such that entire higher groups will be lost. We show here with simulation that phylogenetically clustered extinction risks are necessary but not sufficient for the extensive loss of phylogenetic diversity (PD) compared to random extinction. We simulated Yule trees and evolved extinction risks at various levels of heritability (measured using Pagel's lambda). At most levels of heritability (l in range of 0 to 10), mean values of extinction risk (range 0.25 to 0.75), tree sizes (64 to 128 tips), tree balance and temporal heterogeneity of diversification rates (Yule and coalescent trees), extinction risks do not substantially increase the loss of PD in these trees when compared to random extinction. The maximum loss of PD (20% above random) was only associated with the combination of extremely excessive values of phylogenetic signal, high mean species' extinction probabilities, and extreme (coalescent) tree shapes. Interestingly, we also observed a decline in the rate of increase in the loss of PD at high phylogenetic clustering (l? 10) of extinction risks. Our results suggest that the interplay between various aspects of tree shape and a predisposition of higher extinction risks in species-poor clades is required to explain the substantial pruning of the Tree of Life. DOI
55. Harmon, LJ; Losos, JB; Davies, TJ; Gillespie, RG; Gittleman, JL; Jennings, WB; Kozak, KH; McPeek, MA; Moreno-Roark, F; Near, TJ; Purvis, A; Ricklefs, RE; Schluter, D; Schulte, JA; Seehausen, O; Sidlauskas, BL; Torres-Carvajal, O; Weir, JT; Mooers, AO. (2010) EARLY BURSTS OF BODY SIZE AND SHAPE EVOLUTION ARE RARE IN COMPARATIVE DATA.Evolution 64: 2385-2396 EARLY BURSTS OF BODY SIZE AND SHAPE EVOLUTION ARE RARE IN COMPARATIVE DATA
Adaptive radiation; Brownian motion; comparative methods; model fitting; phylogeny
George Gaylord Simpson famously postulated that much of life's diversity originated as adaptive radiations-more or less simultaneous divergences of numerous lines from a single ancestral adaptive type. However, identifying adaptive radiations has proven difficult due to a lack of broad-scale comparative datasets. Here, we use phylogenetic comparative data on body size and shape in a diversity of animal clades to test a key model of adaptive radiation, in which initially rapid morphological evolution is followed by relative stasis. We compared the fit of this model to both single selective peak and random walk models. We found little support for the early-burst model of adaptive radiation, whereas both other models, particularly that of selective peaks, were commonly supported. In addition, we found that the net rate of morphological evolution varied inversely with clade age. The youngest clades appear to evolve most rapidly because long-term change typically does not attain the amount of divergence predicted from rates measured over short time scales. Across our entire analysis, the dominant pattern was one of constraints shaping evolution continually through time rather than rapid evolution followed by stasis. We suggest that the classical model of adaptive radiation, where morphological evolution is initially rapid and slows through time, may be rare in comparative data. DOI
54. Kuhn, TS; McFarlane, KA; Groves, P; Mooers, AO; Shapiro, B. (2010) Modern and ancient DNA reveal recent partial replacement of caribou in the southwest Yukon.Molecular Ecology 19: 1312-1323 Modern and ancient DNA reveal recent partial replacement of caribou in the southwest Yukon
ancient DNA; caribou; conservation genetics; microsatellite
The long-term persistence of forest-dwelling caribou (Rangifer tarandus caribou) will probably be determined by management and conservation decisions. Understanding the evolutionary relationships between modern caribou herds, and how these relationships have changed through time will provide key information for the design of appropriate management strategies. To explore these relationships, we amplified microsatellite and mitochondrial markers from modern caribou from across the Southern Yukon, Canada, as well as mitochondrial DNA from Holocene specimens recovered from alpine ice patches in the same region. Our analyses identify a genetically distinct group of caribou composed of herds from the Southern Lakes region that may warrant special management consideration. We also identify a partial genetic replacement event occurring 1000 years before present, coincident with the deposition of the White River tephra and the Medieval Warm Period. These results suggest that, in the face of increasing anthropogenic pressures and climate variability, maintaining the ability of caribou herds to expand in numbers and range may be more important than protecting the survival of any individual, isolated sedentary forest-dwelling herd. DOI
53. Kuhn, TS; Mooers, AO. (2010) Missing saiga on the taiga.Molecular Ecology 19: 4834–4836 Missing saiga on the taiga
ancient DNA; Pleistocene; saiga
Conservation biologists understand that linking demographic histories of species at risk with causal biotic and abiotic events should help us predict the effects of ongoing biotic and abiotic change. In parallel, researchers have started to use ancient genetic information (aDNA) to explore the demographic histories of a number of species present in the Pleistocene fossil record (see, e. g. Shapiro et al. 2004). However, aDNA studies have primarily focused on identifying long-term population trends, linked to climate variability and the role of early human activity. Population trends over more recent time, e. g. during the Holocene, have been poorly explored, partly owing to analytical limitations. In this issue, Campos et al. (2010a) highlight the potential of aDNA to investigate demographic patterns over such recent time periods for the compelling and endangered saiga antelope Saiga tatarica (Fig. 1). The time may come when past and current demography can be combined to produce a seamless record. DOI
52. Magnuson-Ford, K; Mooers, A; Paquette, SR; Steel, M. (2010) Comparing strategies to preserve evolutionary diversity.Journal of Theoretical Biology 266: 107-116 Comparing strategies to preserve evolutionary diversity
Extinction; Phylogenetic diversity; Biodiversity conservation
The likely future extinction of various species will result in a decline of two quantities: species richness and phylogenetic diversity (PD, or 'evolutionary history'). Under a simple stochastic model of extinction, we can estimate the expected loss of these quantities under two conservation strategies: An 'egalitarian' approach, which reduces the extinction risk of all species, and a 'targeted' approach that concentrates conservation effort on the most endangered taxa. For two such strategies that are constrained to experience the same expected loss of species richness, we ask which strategy results in a greater expected loss of PD. Using mathematical analysis and simulation, we describe how the strategy (egalitarian versus targeted) that minimizes the expected loss of PD depends on the distribution of endangered status across the tips of the tree, and the interaction of this status with the branch lengths. For a particular data set consisting of a phylogenetic tree of 62 lemur species, with extinction risks estimated from the IUCN 'Red List', we show that both strategies are virtually equivalent, though randomizing these extinction risks across the tip taxa can cause either strategy to outperform the other. In the second part of the paper, we describe an algorithm to determine how extreme the loss of PD for a given decline in species richness can be. We illustrate the use of this algorithm on the lemur tree. (C) 2010 Elsevier Ltd. All rights reserved. DOI
51.Mooers, AO; Doak, DF; Findlay, CS; Green, DM; Grouios, C; Manne, LL; Rashvand, A; Rudd, MA; Whitton, J. (2010) Science, Policy, and Species at Risk in Canada.Bioscience 60 Science, Policy, and Species at Risk in Canada
endangered species; critical habitat; listing; recovery; transparency
The meaningful incorporation of independent scientific advice into effective public policy is a hurdle for any conservation legislation. Canada's Species at Risk Act (SARA; 2002) was designed to separate the science-based determination of a species' risk status from the decision to award it legal protection. However, thereafter, the input of independent science into policy has not been clearly identifiable. Audits of SARA have identified clear deficiencies in the protection and recovery of listed species; for example, of the 176 species legally protected in 2003, only one has a legal implementation plan for its recovery We argue that clearly distinguishing science from policy at all relevant stages would improve the scientific integrity, transparency, accountability, and public acceptance of the legal listing and recovery implementation processes in SARA. Such delineation would also clarify exactly what trade-offs are being made between at-risk species recovery and competing policy objectives. DOI
50. Redding, DW; DeWolff, CV; Mooers, AO. (2010) Evolutionary Distinctiveness, Threat Status, and Ecological Oddity in Primates.Conservation Biology 24: 1052-1058 Evolutionary Distinctiveness, Threat Status, and Ecological Oddity in Primates
conservation priorities; phylogenetic isolation; triage
The EDGE (evolutionarily distinct and globally endangered) conservation program (www.edgeofexistence.org) uses a composite measure of threat and phylogenetic isolation to rank species for conservation attention. Using primates as a test case, we examined how species that rank highly with this metric represent the collective from which they are drawn. We considered the ecological and morphological traits, including body mass, diet, terrestriality, and home range size, of all 233 species of primates. Overall, EDGE score and the level of deviance from the mean of 20 different ecological, reproductive, and morphological variables were correlated (mean correlation r = 0.14, combined p = 1.7 x 10(-14)). Although primates with a high EDGE score had characteristics that made them seem odd, they did not seem to express more ancestral characteristics than expected. Sets of primate species with high EDGE scores will, therefore, collectively capture a broader than expected range of the biology of the clade. If similar patterns hold in other groups, the EDGE metric may be useful for prioritizing biodiversity for conservation. DOI
49. Steel, M; Mooers, A. (2010) The expected length of pendant and interior edges of a Yule tree.Applied Mathematics Letters 23: 1315-1319 The expected length of pendant and interior edges of a Yule tree
Tree; Pure-birth process; Yule model; Differential equation
The Yule (pure-birth) model is the simplest null model of speciation; each lineage gives rise to a new lineage independently with the same rate lambda. We investigate the expected length of an edge chosen at random from the resulting evolutionary tree. In particular, we compare the expected length of a randomly selected edge with the expected length of a randomly selected pendant edge. We provide some exact formulae, and show how our results depend slightly on whether the depth of the tree or the number of leaves is conditioned on, and whether lambda is known or is estimated using maximum likelihood. (C) 2010 Elsevier Ltd. All rights reserved. DOI
48. Warwas, ML; Yeung, JHF; Indurugalla, D; Mooers, AO; Bennet, AJ; Moore, MM. (2010) Cloning and characterization of a sialidase from the filamentous fungus, Aspergillus fumigatus.Glycoconjugate Journal 27: 533-548 Cloning and characterization of a sialidase from the filamentous fungus, Aspergillus fumigatus
Sialidase; Sialic acid; Phylogeny; Fungi N-acetylneuraminic acid; Expression
A gene encoding a putative sialidase was identified in the genome of the opportunistic fungal pathogen, Aspergillus fumigatus. Computational analysis showed that this protein has Asp box and FRIP domains, it was predicted to have an extracellular localization, and a mass of 42 kDa, all of which are characteristics of sialidases. Structural modeling predicted a canonical 6-bladed beta-propeller structure with the model's highly conserved catalytic residues aligning well with those of an experimentally determined sialidase structure. The gene encoding the putative Af sialidase was cloned and expressed in Escherichia coli. Enzymatic characterization found that the enzyme was able to cleave the synthetic sialic acid substrate, 4-methylumbelliferyl alpha-D-N-acetylneuraminic acid (MUN), and had a pH optimum of 3.5. Further kinetic characterization using 4-methylumbelliferyl alpha-D-N-acetylneuraminylgalactopyranoside revealed that Af sialidase preferred alpha 2-3-linked sialic acids over the alpha 2-6 isomers. No trans-sialidase activity was detected. qPCR studies showed that exposure to MEM plus human serum induced expression. Purified Af sialidase released sialic acid from diverse substrates such as mucin, fetuin, epithelial cell glycans and colominic acid, though A. fumigatus was unable to use either sialic acid or colominic acid as a sole source of carbon. Phylogenetic analysis revealed that the fungal sialidases were more closely related to those of bacteria than to sialidases from other eukaryotes. DOI PubMed
46. Magnuson-Ford, K; Ingram, T; Redding, DW; Mooers, AO. (2009) Rockfish (Sebastes) that are evolutionarily isolated are also large, morphologically distinctive and vulnerable to overfishing.Biological Conservation 142: 1787-1796 Rockfish (Sebastes) that are evolutionarily isolated are also large, morphologically distinctive and vulnerable to overfishing
MARINE FISHES; PHYLOGENETIC DIVERSITY; EXTINCTION RISK; BODY-SIZE; FUNCTIONAL DIVERSITY; DIVERSIFICATION; SCORPAENIFORMES; REDESCRIPTION; RESURRECTION; SPECIATION
In an age of triage,me must prioritize species for conservation effort. Species more isolated on the tree of life are candidates for increased attention. The rockfish genus Sebastes is speciose (>100 spp.), morphologically and ecologically diverse and many species are heavily fished. We used a complete Sebastes phylogeny to calculate a measure of evolutionary isolation for each species and compared this to their morphology and imperilment. We found that evolutionarily isolated species in the northeast Pacific are both larger-bodied and, independent of body size, morphologically more distinctive. We examined extinction risk within rockfish using a compound measure of each species' intrinsic vulnerability to overfishing and categorizing species as commercially fished or not. Evolutionarily isolated species in the northeast Pacific are more likely to be fished, and, due to their larger sizes and to life history traits such as long lifespan and slow maturation rate, they are also intrinsically more vulnerable to overfishing. Finally, the set of northeast Pacific species that are both fished and most intrinsically vulnerable to fishing are among the most evolutionarily distinctive. These findings suggest that, at least for this clade, extra attention should be paid to evolutionary distinctiveness when prioritizing species for conservation. (C) 2009 Elsevier Ltd. All rights reserved. DOI
45. Meuser, E; Harshaw, HW; Mooers, AO. (2009) Public Preference for Endemism over Other Conservation-Related Species Attributes.Conservation Biology 23: 1041-1046 Public Preference for Endemism over Other Conservation-Related Species Attributes
BIODIVERSITY; VALUATION; EXTINCTION; ATTITUDES; BENEFITS; POLICY
Public preferences are likely to play an important role in prioritizing species at risk for conservation. We conducted a survey of British Columbians (Canada) (n = 555, r = 73%) to examine how the public ranks a species' attributes (rather than named species) with respect to conservation priority. Endemism, defined as species only or mainly occurring in British Columbia or species occurring in British Columbia and nowhere else in Canada, was considered the most important among the measured attributes. This preference was strongest among men and among respondents who had completed postsecondary education. The preference for endemism is generally consistent with science-based federal listings of British Columbian species. This congruence between listing and public opinion is welcome if such congruence is considered important. We suggest that investigating how much the public values species' attributes, as opposed to named species, provides a more efficient way of incorporating public opinion into policies on species at risk, especially if large numbers of species must be ranked for conservation priority. DOI
44.Mooers, AO; Redding, DW. (2009) Where the rare species are.Molecular Ecology 18: 3955-3957 Where the rare species are
BIODIVERSITY; DIVERSITY
Prioritizing geographic areas for conservation attention is important - time and money are in short supply but endangered species are not - and difficult. One popular perspective highlights areas with many species found nowhere else (Myers et al. 2000). Another identifies areas that contain species with fewer close relatives elsewhere (Faith 1992). One might characterize the first as focusing on geographic, and the second on phylogenetic, rarity. To the extent that geographically rare species are at greater risk of extinction (Gaston & Fuller 2009), and that phylogenetically rare species contribute disproportionally to overall biodiversity (Crozier 1997), it would seem reasonable to formally integrate the two approaches. In this issue, Rosauer et al. (2009) do just that; their elegant combined metric pinpoints areas missed out when the two types of rarity are looked at in isolation. DOI
43. Lee, V; Huang, JL; Lui, MF; Malecek, K; Ohta, Y; Mooers, A; Hsu, E. (2008) The evolution of multiple isotypic IgM heavy chain genes in the shark.Journal of Immunology 180: 7461-7470 The evolution of multiple isotypic IgM heavy chain genes in the shark
PHYLOGENETICALLY PRIMITIVE VERTEBRATE; CONSTANT-REGION GENES; NURSE SHARK; GINGLYMOSTOMA-CIRRATUM; SOMATIC HYPERMUTATION; IMMUNOGLOBULIN GENES; MOUSE; DIVERSIFICATION; ORGANIZATION; EXPRESSION
The IgM H chain gene organization of cartilaginous fishes consists of 15-200 miniloci, each with a few gene segments (V-H-D1-D2-J(H)) and one C gene. This is a gene arrangement ancestral to the complex IgH locus that exists in all other vertebrate classes. To understand the molecular evolution of this system, we studied the nurse shark, which has relatively fewer loci, and characterized the IgH isotypes for organization, functionality, and the somatic diversification mechanisms that act upon them. Gene numbers differ slightly between individuals (similar to 15), but five active IgM subclasses are always present. Each gene undergoes rearrangement that is strictly confined within the minilocus; in B cells there is no interaction between adjacent loci located; >= 120 kb apart. Without combinatorial events, the shark IgM H chain repertoire is based on junctional diversity and, subsequently, somatic hypermutation. We suggest that the significant contribution by junctional diversification reflects the selected novelty introduced by RAG in the early vertebrate ancestor, whereas combinatorial diversity coevolved with the complex translocon organization. Moreover, unlike other cartilaginous fishes, there are no germline-joined VDJ at any nurse shark mu locus, and we suggest that such genes, when functional, are species-specific and may have specialized roles. With an entire complement of IgM genes available for the first time, phylogenetic analyses were performed to examine how the multiple Ig loci evolved. We found that all domains changed at comparable rates, but V-H appears to be under strong positive selection for increased amino acid sequence diversity, and surprisingly, so does C mu 2.
42.Mooers, AO; Faith, DP; Maddison, WP. (2008) Converting Endangered Species Categories to Probabilities of Extinction for Phylogenetic Conservation Prioritization.PLOS One 3: e700. Converting Endangered Species Categories to Probabilities of Extinction for Phylogenetic Conservation Prioritization
Background: Categories of imperilment like the global IUCN Red List have been transformed to probabilities of extinction and used to rank species by the amount of imperiled evolutionary history they represent ( e. g. by the Edge of Existence programme). We investigate the stability of such lists when ranks are converted to probabilities of extinction under different scenarios. Methodology and Principal Findings: Using a simple example and computer simulation, we show that preserving the categories when converting such list designations to probabilities of extinction does not guarantee the stability of the resulting lists. Significance: Care must be taken when choosing a suitable transformation, especially if conservation dollars are allocated to species in a ranked fashion. We advocate routine sensitivity analyses.Website DOI
41. Redding, DW; Hartmann, K; Mirnoto, A; Bokal, D; Devos, M; Mooers, AO. (2008) Evolutionarily distinctive species often capture more phylogenetic diversity than expected.J. Theor. Biol. 251: 606-615 Evolutionarily distinctive species often capture more phylogenetic diversity than expected
conservation priorities; distinctiveness; evolutionary value; genetic uniqueness
Evolutionary distinctiveness measures of how evolutionarily isolated a species is relative to other members of its clade. Recently, distinctiveness metrics that explicitly incorporate time have been proposed for conservation prioritization. However, we found that such measures differ qualitatively in how well they capture the total amount of evolution (termed phylogenetic diversity, or PD) represented by a set of species. We used simulation and simple graph theory to explore this relationship with reference to phylogenetic tree shape. Overall, the distinctiveness measures capture more PD on more unbalanced trees and on trees with many splits near the present. The rank order of performance was robust across tree shapes, with apportioning measures performing best and node-based measures performing worst. A sample of 50 ultrametric trees from the literature showed the same patterns. Taken together, this suggests that distinctiveness metrics may be a useful addition to other measures of value for conservation prioritization of species. The simplest measure, the age of a species, performed surprisingly well, suggesting that new measures that focus on tree shape near the tips may provide a transparent alternative to more complicated full-tree approaches. (c) 2008 Elsevier Ltd. All rights reserved. DOI PubMed
40. Kolm, N; Stein, RW; Mooers, AO; Verspoor, JJ; Cunningham, EJA. (2007) Can sexual selection drive female life histories? A comparative study on Galliform birds.Journal of Evolutionary Biology 20: 627-638 Can sexual selection drive female life histories? A comparative study on Galliform birds
body size; clutch size; Discrete; egg size; mating system; sexual size dimorphism; supertree phylogeny; trade-off
Sexual selection has been identified as a major evolutionary force shaping male life history traits but its impact on female life history evolution is less clear. Here we examine the impact of sexual selection on three key female traits (body size, egg size and clutch size) in Galliform birds. Using comparative independent contrast analyses and directional DISCRETE analyses, based on published data and a new genera-level supertree phylogeny of Galliform birds, we investigated how sexual selection [quantified as sexual size dimorphism (SSD) and social mating system (MS)] affects these three important female traits. We found that female body mass was strongly and positively correlated with egg size but not with clutch size, and that clutch size decreased as egg size increased. We established that SSD was related to MS, and then used SSD as a proxy of the strength of sexual selection. We found both a positive relationship between SSD and female body mass and egg size and that increases in female body mass and egg size tend to occur following increases in SSD in this bird order. This pattern of female body mass increases lagging behind changes in SSD, established using our directional DISCRETE analysis, suggests that female body mass increases as a response to increases in the level of sexual selection and not simply through a strong genetic relationship with male body mass. This suggests that sexual selection is linked to changes in female life history traits in Galliformes and we discuss how this link may shape patterns of life history variation among species. DOI
35. Parker, JDK; Bradley, BA; Mooers, AO; Quarmby, LM. (2007) Phylogenetic Analysis of the Neks Reveals Early Diversification of Ciliary-Cell Cycle Kinases.PLoS One 2 Phylogenetic Analysis of the Neks Reveals Early Diversification of Ciliary-Cell Cycle Kinases
Background. NIMA-related kinases (Neks) have been studied in diverse eukaryotes, including the fungus Aspergillus and the ciliate Tetrahymena. In the former, a single Nek plays an essential role in cell cycle regulation; in the latter, which has more than 30 Neks in its genome, multiple Neks regulate ciliary length. Mammalian genomes encode an intermediate number of Neks, several of which are reported to play roles in cell cycle regulation and/or localize to centrosomes. Previously, we reported that organisms with cilia typically have more Neks than organisms without cilia, but were unable to establish the evolutionary history of the gene family. Methodology/Principle Findings. We have performed a large-scale analysis of the Nek family using Bayesian techniques, including tests of alternate topologies. We find that the Nek family had already expanded in the last common ancestor of eukaryotes, a ciliated cell which likely expressed at least five Neks. We suggest that Neks played an important role in the common ancestor in regulating cilia, centrioles, and centrosomes with respect to mitotic entry, and that this role continues today in organisms with cilia. Organisms that lack cilia generally show a reduction in the number of Nek clades represented, sometimes associated with lineage specific expansion of a single clade, as has occurred in the plants. Conclusion/Significance. This is the first rigorous phylogenetic analysis of a kinase family across a broad array of phyla. Our findings provide a coherent framework for the study of Neks and their roles in coordinating cilia and cell cycle progression.Website DOI PubMed
34. Rundle, HD; Odeen, A; Mooers, AO. (2007) An experimental test for indirect benefits in Drosophila melanogaster.BMC Evolutionary Biology 7 An experimental test for indirect benefits in Drosophila melanogaster
Background: Despite much empirical attention, tests for indirect benefits of mate choice have rarely considered the major components of sexual and nonsexual offspring fitness relevant to a population. Here we use a novel experimental design to test for the existence of any indirect benefits in a laboratory adapted population of D. melanogaster. Our experiment compared the fitness (mating success, longevity, and productivity) of individuals possessing genomes that derived two generations previously from males that were either entirely successful (studs) or wholly unsuccessful (duds) at achieving mates in three subsequent rounds of mating trials. Results: Males from the stud treatment were 30% more successful on average at securing mates than males from the dud treatment. In contrast, we found no difference between treatments in measures of productivity or of longevity when measured in a mixed-sex environment. In the absence of females, however, males in the stud treatment outlived males in the dud treatment. Conclusion: Our results suggest that mating with successful males in this population provides an indirect benefit to females and that, at least in this environment, the benefit arises primarily through the production of more attractive male offspring. However, it is unclear whether this represents solely a traditional sexy sons benefit or whether there is an additional good genes component (with male offspring simply allocating their surplus condition to traits that enhance their mating success). The lack of any detectable differences in female fitness between the two treatments suggests the former, although the longevity advantage of males in the stud treatment when females were absent is consistent with the latter. Determining the effect of this indirect benefit on the evolution of female mate preferences (or resistance) will require comparable data on the direct costs of mating with various males, and an understanding of how these costs and benefits integrate across generations and vary among environments. DOI
32. Charrette, NA; Cleary, DFR; Mooers, AO. (2006) Range-restricted, specialist Bornean butterflies are less likely to recover from enso-induced disturbance.Ecology 87: 2330-2337 Range-restricted, specialist Bornean butterflies are less likely to recover from enso-induced disturbance
El Nino; endemic; extirpation; forest fire; generalist; geographic range; specialist
The forest. res induced by the El Nino Southern Oscillation ( ENSO) in 1997 1998 resulted in the temporary extirpation of more than 100 lowland butterfly species at a forest site in Borneo. Species with more restricted ranges were less likely to recover over the following four years. Matched-pair analyses revealed that species with lower initial abundances, restricted geographic ranges, and more specialized larvae were less likely to return. Specialization differed predictably between the ( more generalist) wide-range and ( more specialized) restricted- range species in our data set, and both geographic range and level of specialization were important in multivariate models. These are the first observations directly linking extent of occurrence, ecological specialization, and observed recovery following local extirpation. If recovery time exceeds the frequency of disturbance, local extirpation can lead to local extinction. Given that ENSO-induced disturbances are increasing in frequency, in severity, and in geographic scale, these results suggest that specialist species with restricted geographic ranges could be at particularly high risk of global extinction.
31. Cleary, DFR; Fauvelot, C; Genner, MJ; Menken, SBJ; Mooers, AO. (2006) Parallel responses of species and genetic diversity to El Nino Southern Oscillation-induced environmental destruction.Ecology Letters 9: 301-307 Parallel responses of species and genetic diversity to El Nino Southern Oscillation-induced environmental destruction
Species diversity within communities and genetic diversity within species are two fundamental levels of biodiversity. Positive relationships between species richness and within-species genetic diversity have recently been documented across natural and semi-natural habitat islands, leading Vellend to suggest a novel macro-ecological pattern termed the species-genetic diversity correlation. We tested whether this prediction holds for areas affected by recent habitat disturbance using butterfly communities in east Kalimantan, Indonesia. Here, we show that both strong spatial and temporal correlations exist between species and allelic richness across rainforest habitats affected by El Nino Southern Oscillation-induced disturbance. Coupled with evidence that changes in species richness are a direct result of local extirpation and lower recruitment, these data suggest that forces governing variation at the two levels operate over parallel and short timescales, with implications for biodiversity recovery following disturbance. Remnant communities may be doubly affected, with reductions in species richness being associated with reductions in genetic diversity within remnant species.PDF
30. Cleary, DFR; Mooers, AO. (2006) Burning and logging differentially affect endemic vs. widely distributed butterfly species in Borneo.Divers Distrib 12: 409-416 Burning and logging differentially affect endemic vs. widely distributed butterfly species in Borneo
abundance; El Nino; disturbance; endemism; extirpation; fire
We assess the differential impact of logging and ENSO (El Nino Southern Oscillation)-induced disturbance on the relative butterfly abundance and species richness of range-restricted and widespread species within the island of Borneo. Relative abundance and species richness were assessed using rarefaction and species accumulation curves in unburned isolates surrounded by burned forest, the burned forest itself, and continuous forest unaffected by ENSO-induced disturbance in addition to logged and unlogged landscapes in unburned forest. The relative abundance of endemics was significantly higher in unlogged forest than logged forest and significantly higher in unburned forest than burned forest. Rarefied species richness of range categories was similar (Bornean endemics) or higher (other categories) in selectively logged than unlogged forest. In contrast, rarefied species richness of range-restricted species was highest in continuous forest, intermediate in unburned isolates, and lowest in burned forest. Only two individuals of a single Bornean endemic species were found in all the burned forest. Although species richness was higher in all range categories in continuous forest than in unburned isolates and in burned forest, the difference was most pronounced for range-restricted species. Logging and ENSO-induced fires thus have contrasting effects on range-restricted species. While both increase the relative abundance of widely distributed species at the expense of range-restricted species, only ENSO-induced disturbance lowers the rarefied number of restricted range species. Our research highlights the threat that severe ENSO events pose to geographically restricted classes of biodiversity.
29. Lee, CH; Blay, S; Mooers, AO; Singh, A; Oakley, TH. (2006) CoMET: A Mesquite package for comparing models of continuous character evolution on phylogenies.Evolutionary Bioinformatics 2: 183-186 CoMET: A Mesquite package for comparing models of continuous character evolution on phylogenies
Maximum likelihood; Brownian motion; continuous traits; phylogeny
Continuously varying traits such as body size or gene expression level evolve during the history of species or gene lineages. To test hypotheses about the evolution of such traits, the maximum likelihood (ML) method is often used. Here we introduce CoMET (Continuous-character Model Evaluation and Testing), which is module for Mesquite that automates likelihood computations for nine different models of trait evolution. Due to its few restrictions on input data, CoMET is applicable to testing a wide range of character evolution hypotheses. The CoMET homepage, which links to freely available software and more detailed usage instructions, is located at http://www.lifesci.ucsb.edu/eemb/labs/oakley/software/comet.htm.
28. Redding, DW; Mooers, AO. (2006) Incorporating evolutionary measures into conservation prioritization.Conservation Biology 20: 1670-1678 Incorporating evolutionary measures into conservation prioritization
birds; evolutionary worth; global avifauna; IUCN Red List; phylogenetic diversity; threatened species
Conservation prioritization is dominated by the threat status of candidate species. However, species differ markedly in the shared genetic information they embody, and this information is not taken into account if species are prioritized by threat status alone. We developed a system of prioritization that incorporates both threat status and genetic information and applied it to 9546 species of birds worldwide. We devised a simple measure of a species' genetic value that takes into account the shape of the entire taxonomic tree of birds. This measure approximates the evolutionary history that each species embodies and sums to the phylogenetic diversity of the entire taxonomic tree. We then combined this genetic value with each species' probability of extinction to create a species-specific measure of expected loss of genetic information. The application of our methods to the world's avifauna showed that ranking species by expected loss of genetic information may help preserve bird evolutionary history by upgrading those threatened species with fewer close relatives. We recommend developing a mechanism to incorporate a species' genetic value into the prioritization framework.Website DOI
27. Drake, A; Rashkovetsky, E; Wong, D; Rundle, HD; Mooers, AO. (2005) Variable assortative mating in replicate mating trials using Drosophila melanogaster populations derived from contrasting opposing slopes of 'Evolution Canyon', Israel.Journal of Evolutionary Biology 18: 1123-1129 Variable assortative mating in replicate mating trials using Drosophila melanogaster populations derived from contrasting opposing slopes of 'Evolution Canyon', Israel
behavioural isolation; ecological speciation; mate choice; mating preferences; premating isolation
Significant assortative mating in laboratory studies has been previously shown between two populations of Drosophila melanogaster collected from micro-climactically contrasting and opposing slopes of 'Evolution Canyon' (Lower Nahal Oren, Israel; Korol et al., 2000). Coupled with evidence that the two populations are adapted to their respective environments, this has been suggested as a rare example of ongoing behaviourally mediated speciation occurring in the face of gene flow. Reproductive isolation between these populations, however, has never been confirmed by replicate experiments in an independent laboratory. For this reason, we tested recent collections of these populations for premating isolation in both the original (Haifa) and a new (Burnaby) laboratory under a variety of experimental protocols. Although non-random mating was found in the majority of trials conducted in Haifa, we were unable to replicate these strong results in Burnaby. Most notably, we failed to detect assortative mating in four separate double choice experiments. Significant non-random mating was detected, however, in three of six single choice experiments in Burnaby, suggesting that the populations are behaviourally differentiated in some manner. Why nonrandom mating was weaker in Burnaby than Haifa is not understood, but suggests that assortative mating may be sensitive to unknown environmental factors.PDF
26. Lewis, RL; Beckenbach, AT; Mooers, AO. (2005) The phylogeny of the subgroups within the melanogaster species group: Likelihood tests on COI and COII sequences and a Bayesian estimate of phylogeny.Molecular Phylogenetics and Evolution 37: 15-24 The phylogeny of the subgroups within the melanogaster species group: Likelihood tests on COI and COII sequences and a Bayesian estimate of phylogeny
Drosophila melanogaster; takahashii; suzukii; ananassae; montium; COI; COII; phylogeny; likelihood; ratchet; bayesphylogenies
The relationships among the majority of the subgroups in the Drosophila melanogaster species group remain unresolved. We present a 2223 basepair dataset for mitochondrial cytochrome oxidase I and cytochrome oxidase H for 43 species (including new data from II species), sampled to include the major subgroups. After a brief review of competing hypotheses for the ananassae, montium, suzukii, and takahashii subgroups, we combine the two genes based on a new use of the SH test and present KH and SH likelihood comparisons (Kishino and Hasegawa, 1989. J. Mol. Evol. 29, 170-179; Shimodaira and Hasegawa, 1999) to test the monophyly and placement of these subgroups within the larger species group. Although we find insignificant differences between the two suggested placements for the ananassae subgroup, the ananassae is sister to the rest of the subgroups in the melanogaster species group in every investigation. For the takahashii subgroup, although we cannot reject monophyly, the species are so closely related to the suzukii subgroup for these data that the two subgroups often form one clade. Finally, we present a Bayesian estimate of the phylogeny for both genes combined, utilizing a recently published method that allows for different models of evolution for different sites. (c) 2005 Elsevier Inc. All rights reserved.PDF
25. Nosil, P; Mooers, AO. (2005) Testing hypotheses about ecological specialization using phylogenetic trees.Evolution 59: 2256-2263 Testing hypotheses about ecological specialization using phylogenetic trees
ancestral state reconstruction; ecological specialization; maximum likelihood; phytophagous insects; transition rates; sensitivity analysis
It is often assumed that ecological specialization represents an evolutionary "dead-end" that limits further evolution. Maximum-likelihood (ML) analyses on phylogenies for 15 groups of phytophagous insects revealed that high transition rates both to and from specialization occurred, but that the mean ratio of rates was significantly biased toward a higher rate to specialization. Here we explore the consequences of the fact that transition rates inferred by ML are affected not only by the distribution, but also by the frequency, of character states. Higher rates to the more common state were inferred in the analyses of Nosil (2002), in similar studies published since 2002, and in a small set of simulations. Thus, the ratio of the rate toward versus away from specialization was strongly, positively correlated with the proportion of specialist species at the tips of the phylogeny and whether transitions away from specialization occur remains unclear. Here we reexamine these data using methods that do not rely on directly comparing transition rates. Maximum-likelihood analyses show that models with no transitions in one direction (e.g., irreversible evolution as predicted by the "specialist as dead end" framework) are usually strongly rejected, independent of the proportion of specialists at the tips. Ancestral state reconstruction revealed two instances where generalists were unambiguously derived from specialists. Transition rates would need to biased 100-fold and 5000-fold toward specialization to reconstruct a history where these shifts from specialization toward generalization do not occur. The general conclusions of Nosil (2002) appear to hold; transitions in either direction likely occur such that specialization does not always limit further evolution. Most generally, inferences regarding character evolution can be strengthened by comparing models of character change and examining ancestor states, rather than only comparing parameter values.PDF
24. Soutullo, A; Dodsworth, S; Heard, SB; Mooers, AO. (2005) Distribution and correlates of carnivore phylogenetic diversity across the Americas.Animal Conservation 8: 249-258 Distribution and correlates of carnivore phylogenetic diversity across the Americas
Digital maps and a dated supertree of global carnivore species were used to assess the distribution of American carnivores' phylogenetic diversity (PD, measured in millions of years) both from a geopolitical perspective ('evolutionary heritage' or EH) and on the basis of species' range size and conservation status. A new measure, range-weighted EH, is introduced. This measure partitions the total PD of the tree between countries based on the proportion of species' ranges within each country. Sociopolitical correlates of these measures were explored. Only 3% of the total PD in the Americas is endemic to any one country. As expected, the measures of PD are positively correlated with each other and with species richness. The USA contains the most species, the most EH and the second most range-weighted EH after Brazil. Indeed, larger and richer countries, and those with the lowest state-corruption-rate hold most EH. No significant differences were observed in the amount of PD remaining if species are removed at random, or following more plausible sequences based on IUCN conservation status and range size. Eighty percent of the American carnivores' PD would remain safe if only the set of not threatened species were to remain. Roughly the same is true if only the 50% most widespread species were to persist. Samples of wide-ranging species represent more of the entire tree than do samples of narrow-ranging species, highlighting the importance of the former for conservation strategies. We suggest that similar approaches be applied to more groups across the globe to assess which countries and areas steward the most PD, as well as which species and taxa do, in order to plan conservation actions consequently.PDF
23. Cleary, DFR; Mooers, AO. (2004) Butterfly species richness and community composition in forests affected by ENSO-induced burning and habitat isolation in Borneo.Journal of Tropical Ecology 20: 359-367 Butterfly species richness and community composition in forests affected by ENSO-induced burning and habitat isolation in Borneo
El Niho Southern Oscillation; Hesperiidae; Kalimantan; Lycaenidae; Nymphalidae
Landscape-scale studies of community traits such as species richness and community composition are sorely needed to explore the impact of large-scale disturbance events such as ENSO (El Nino Southern Oscillation)-induced burning and habitat isolation on rain-forest communities. Here we assess butterflies in continuous forest, in unburned isolates surrounded by burned forest and in burned forest, in addition to areas sampled before the most recent (1997/98) large-scale burn event in Borneo. Overall levels of species richness were significantly higher pre-ENSO and in continuous forest than in unburned isolates and burned forest. There was, however, some variation among butterfly families in these patterns, with no significant differences among habitats (continuous forest, isolates and burned forest) for the Hesperiidae and significant differences for the other butterfly families. Patterns of community composition showed that similarity was greater between distant continuous forest and isolates than between either of these and burned forest. Since the unburned isolates were surrounded by the burned forest this indicates that the habitat (burned or unburned) overrides geographical differences. Dominant species that contributed substantially to differences among habitats were often completely absent from either burned or unburned forest. The combined patterns of species richness and community structure suggest that burning affects forest ecosystems by a replacement of dominant species while habitat isolation may affect areas by leading to the local extinction of rare species.PDF
22. Cleary, DFR; Mooers, AO; Eichhorn, KAO; van Tol, J; de Jong, R; Menken, SBJ. (2004) Diversity and community composition of butterflies and odonates in an ENSO-induced fire affected habitat mosaic: a case study from East Kalimantan, Indonesia.Oikos 105: 426-446 Diversity and community composition of butterflies and odonates in an ENSO-induced fire affected habitat mosaic: a case study from East Kalimantan, Indonesia
Little is known about the diversity of tropical animal communities in recently fire-affected environments. Here we assessed species richness, evenness, and community similarity of butterflies and odonates in landscapes located in unburned isolates and burned areas in a habitat mosaic that was severely affected by the 1997/98 ENSO (El Nino Southern Oscillation) event in east Kalimantan, Indonesian Borneo. In addition related community similarity to variation in geographic distance between sampling sites and the habitat/vegetation structure Species richness and evenness differed significantly among landscapes but there was no congruence between both taxa. The species richness of butterflies was, for example, highest in sites located in a very large unburned isolate whereas odonate species richness was highest in sites located in a small unburned isolate and once-burned forest. We also found substantial variation in the habitat/vegetation structure among landscapes but this was mainly due to variation between unburned and burned landscapes and variation among burned landscapes. Both distance and environment (habitat/vegetation) contributed substantially to explaining variation in the community similarity (beta diversity) of both taxa. The contribution of the environment was, however, mainly due to variation between unburned and burned landscapes, which contained very different assemblages of both taxa. Sites located in the burned forest contained assemblages that were intermediate between assemblages from sites in unburned forest and sites from a highly degraded slash-and-burn area indicating that the burned forest was probably recolonised by species from these disparate environments. We, furthermore, note that in contrast to species richness (alpha diversity) the patterns of community similarity (beta diversity) were highly congruent between both taxa. These results indicate that community-wide multivariate measures of beta diversity are more consistent among taxa and more reliable indicators of disturbance, such as ENSO-induced burning, than univariate measures.PDF
20. Dukas, R; Mooers, AO. (2003) Environmental enrichment improves mating success in fruit flies.Animal Behaviour 66: 741-749 Environmental enrichment improves mating success in fruit flies
Environmental enrichment, defined as housing conditions that include a combination of complex inanimate and social stimulation, has strong positive effects on brain and behaviour in various species. We extended previous studies to evaluate how enrichment affects mating success. In a series of experiments, we found that male fruit flies, Drosophila melanogaster, reared in an enriched environment were twice as successful in acquiring mates as were males from standard rearing conditions. The dominant factor increasing mating success was the larger space available per fly. Flies from enriched and standard environments showed no significant behavioural differences, leading us to suggest that different social environments at high and low per capita spaces are associated, on average, with either subtle behavioural differences or distinct pheromonal profiles to which females are sensitive while choosing mates. (C) 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.PDF
19.Mooers, AO; Atkins, RA. (2003) Indonesia's threatened birds: over 500 million years of evolutionary heritage at risk.Animal Conservation 6: 183-188 Indonesia's threatened birds: over 500 million years of evolutionary heritage at risk
Using published IUCN red-lists for the threatened bird species of Indonesia (Stattersfield & Capper, 2000), we document that the species at risk in Indonesia are not a taxonomically random sample, consistent with patterns seen at the global scale (Purvis et al., 2000). This implies that a greater than random proportion of Indonesia's and the world's (through the loss of endemics) phylogenetic diversity (PD) is at risk (Von Euler, 2001). Using cytochrome b (Johns & Avise, 1998) and a distance-based taxonomy. we attempt to quantify this projected loss of PD in millions of years and conclude with a brief discussion of the conservation implications for Indonesia, and of the use of 'evolutionary heritage' as a measure for conservation at the geopolitical level.PDF
18. Heard, SB; Mooers, AO. (2002) Signatures of random and selective mass extinctions in phylogenetic tree balance.Systematic Biology 51: 889-897 Signatures of random and selective mass extinctions in phylogenetic tree balance
biodiversity; mass extinction; phylogeny; speciation; tree balance
Current models of diversification with evolving speciation rates have trouble mimicking the extreme imbalance seen in estimated phylogenies. However, these models have not incorporated extinction. Here, we report on a simple simulation model that includes heritable and evolving speciation rates coupled with mass extinctions, Random (but not selective) mass extinctions, coupled with evolving among-lineage variation in speciation rates, increase imbalance of postrecovery clades. Thus, random mass extinctions are plausible contributors to the imbalance of modern clades. Paleontological evidence suggests that mass extinctions are often random with respect to ecological and morphological traits, consistent with our simulations. In contrast, evidence that the current anthropogenic mass extinction is phylogenetically selective suggests that the current extinction episode may be qualitatively different from past ones in the way it reshapes future biotas.
17.Mooers, AH; Heard, SB. (2002) Using tree shape.Systematic Biology 51: 833-834 Using tree shape
PDF
16. Savolainen, V; Heard, SB; Powell, MP; Davies, TJ; Mooers, AO. (2002) Is cladogenesis heritable?Systematic Biology 51: 835-843 Is cladogenesis heritable?
branch length; cladogenesis; diversification; molecular clock; phylogenetic tree shape; speciation
The heritability of speciation rates and extinction risks is a crucial parameter in models of macroevolution, but little direct evidence has been available to assess the occurrence, strength, or generality of this heritability. We tested for heritability using correlations between ancestral and descendent branch lengths in phylogenetic trees, an approach first applied to a bird phylogeny by Harvey et al. (1991, pages 123-137 in Genes in ecology [R. J. Berry et al., eds.], Blackwell Scientific, Oxford). We applied Harvey et al.'s test to some of the largest DNA sequence-based phylogenetic analyses published to date for plants, insects, fungi, and bacteria.. If one of two parent lineages splits first and if this is the case for any heritable reason, then on average we expect its daughter lineages to also split first. We also used a randomization procedure to assess significance of branch length heritability Using maximum parsimony and maximum likelihood branch lengths and trees made ultrametric after nonparametric rate smoothing or by enforcing a molecular clock, we found a pattern for most clades consistent with heritable net cladogenesis. Heritability of cladogenesis maybe a general phenomenon, detectable across a large number of lineages and a broad range of taxa.PDF
14. Heard, SB; Mooers, AO. (2000) Phylogenetically patterned speciation rates and extinction risks change the loss of evolutionary history during extinctions.Proceedings of the Royal Society of London Series B-Biological Sciences 267: 613-620 Phylogenetically patterned speciation rates and extinction risks change the loss of evolutionary history during extinctions
biodiversity; biodiversity calculus; evolutionary history; extinction; phylogenetic tree shape; branch lengths
If we are to plan conservation strategies that minimize the loss of evolutionary history through human-caused extinctions, we must understand how this loss is related to phylogenetic patterns in current extinction risks and past speciation rates. Nee & May (1997, Science 278, 692-694) showed that for a randomly evolving clade (i) a single round of random extinction removed relatively little evolutionary history, and (ii) extinction management (choosing which taxa to sacrifice) offered only marginal improvement. However, both speciation rates and extinction risks vary across lineages within real clades. We simulated evolutionary trees with phylogenetically patterned speciation rates and extinction risks (closely related lineages having similar rates and risks) and then subjected them to several biologically informed models of extinction. Increasing speciation rate variation increases the extinction-management pay-off. When extinction risks vary among lineages but are uncorrelated with speciation rates, extinction removes more history (compared with random trees), but the difference is small. When extinction risks vary and are correlated with speciation rates, history loss can dramatically increase (negative correlation) or decrease (positive correlation) with speciation rate variation. The loss of evolutionary history via human-caused extinctions may therefore be more severe, yet more manageable, than first suggested.PDF
13.Mooers, AO; Holmes, EC. (2000) The evolution of base composition and phylogenetic inference.Trends in Ecology & Evolution 15: 365-369 The evolution of base composition and phylogenetic inference
Base composition varies at all levels of the phylogenetic hierarchy and throughout the genome, and can be caused by active selection or passive mutation pressure. This variation can make reconstructing trees difficult. However, recent tree-based analyses have shed light on the forces responsible for the evolution of base composition, forces that might be very general. More explicit tree-based work is encouraged.
9. Rundle, HD; Mooers, AO; Whitlock, MC. (1999) Experimental tests of founder-flush: A reply to Templeton.Evolution 53: 1632-1633 Experimental tests of founder-flush: A reply to Templeton
bottleneck; Drosophila; founder-flush; genetic transilience; speciation
8.Mooers, AO; Schluter, D. (1998) Fitting macroevolutionary models to phyllogenies: an example using vertebrate body sizes.Contributions to Zoology 68: 3-18 Fitting macroevolutionary models to phyllogenies: an example using vertebrate body sizes
Brownian motion; macroevolution; maximum likelihood; phylogenies; vertebrate body size; evolution
How do traits change through time and with speciation? We present a simple and generally applicable method for comparing various models of the macroevolution of traits within a maximum likelihood framework. We illustrate four such models: 1) variance among species accumulates in direct proportion to time separating them (gradual model); 2) variation accumulates with the number of speciation events separating them (speciational model); 3) differences between species are unrelated to phylogenetic relatedness (pitchfork model); and 4) a free model where the trait evolves at its own idiosyncratic rate among lineages. Using species-specific body size, we compare the four models across two data sets: twenty-one clades of vertebrate species, and two clades of bird families. For the twenty-one vertebrate trees, the pitchfork model is most successful, though not significantly, and the most successful by far for the youngest clades. The speciational model seems to be preferred for older clades. For both clades of bird families, the speciational model offers the best fit to family-level body size evolution. However, the pitchfork model does much worse for one clade than for the other, suggesting a difference in the relationship between diversification and body-size evolution in the two groups. These examples highlight some possibilities afforded by this simple approach.
7. Rundle, HD; Mooers, AO; Whitlock, MC. (1998) Single founder-flush events and the evolution of reproductive isolation.Evolution 52: 1850-1855 Single founder-flush events and the evolution of reproductive isolation
bottleneck; Drosophila; founder-flush; premating isolation; speciation
By demonstrating the evolution of significant premating isolation, previous laboratory experiments have provided some evidence for the founder-flush model of speciation. However, these experiments are subject to a number of criticisms, including the use of hybrid populations recently collected from the wild and the use of multiple bottlenecks. Here we present the results of a test of founder-flush speciation using a single, well-adapted laboratory stock of Drosophila melanogaster subjected to one founder-flush event. The experiment was replicated at larger scale than previous studies, and results indicate that none of 50 independent founder-flush lines evolved significant assortative mating relative to the control (base) population. This suggests a diminished emphasis on population bottlenecks in speciation of D. melanogaster and perhaps in general.
6. Bell, G; Mooers, AO. (1997) Size and complexity among multicellular organisms.Biological Journal of the Linnean Society 60: 345-363 Size and complexity among multicellular organisms
development; differentiation; histology; complexity; evolution; economic biology; division of labour; allometry
The diversity of specialized cell types ('complexity') is estimated for a wide range of multicellular organisms. Complexity increases with size, independently of phylogeny. This is interpreted in economic terms as the consequence of a greater degree of cooperative division of labour within larger entities. The late of increase of complexity with size is less in the case of a cooperative division of labour (cell types within bodies) than in the analogous case of a competitive division of labour (species within communities). This is atttributed to the inutility of single specialized cells whose goods must be shared among all the many cells of a large organism. Major groups of organisms differ in complexity at given size: animals are more complex than plants, and phaeophytes are simpler than either. (C) 1997 The Linnean Society of London.PDF
5.Mooers, AO; Heard, SB. (1997) Evolutionary process from phylogenetic tree shape.Quarterly Review of Biology 72: 31-54 Evolutionary process from phylogenetic tree shape
Inferences about macroevolutionary process have traditionally depended solely on the fossil record, but such inferences can be strengthened by also considering the shapes of the phylogenetic trees that link extant taxa. The realization that phylogenies reflect macroevolutionary processes has fed to a growing literature of theoretical and comparative studies of tree shape. Two aspects of tree shape are particularly important: tree balance and the distribution of branch lengths. We examine and evaluate recent developments in and connections between these two aspects, and suggest directions for future research. Studies of tree shape promise useful and powerful tests of macroevolutionary hypotheses. With appropriate further research, tree shape may help us detect mass extinctions and adaptive radiations, measure continuous variation in speciation and extinction rates, and associate changes in these rates with ecological or biogeographical causes. The usefulness of tree shape extends well beyond the study of macroevolution. We discuss applications to other areas of biology, including coevolution, phylogenetic inference, population biology, and developmental biology.
4. Schluter, D; Price, T; Mooers, AO; Ludwig, D. (1997) Likelihood of ancestor states in adaptive radiation.Evolution 51: 1699-1711 Likelihood of ancestor states in adaptive radiation
adaptive radiation; ancestor states; maximum likelihood; evolution of specialization; phylogeny
Theories of ecological diversification make predictions about the timing and ordering of character state changes through history. These theories are testable by "reconstructing" ancestor states using phylogenetic trees and measurements of contemporary species. Here we use maximum likelihood to estimate and evaluate the accuracy of ancestor reconstructions. We present likelihoods of discrete ancestor states and derive probability distributions for continuous ancestral traits. The methods are applied to several examples: diets of ancestral Darwin's finches; origin of inquilinism in gall wasps; microhabitat partitioning and body size evolution in scrubwrens; digestive enzyme evolution in artiodactyl mammals; origin of a sexually selected male trait, the sword, in platies and swordtails; and evolution of specialization in Anolis lizards. When changes between discrete character states are rare, the maximum likelihood results are similar to parsimony estimates. In this case the accuracy of estimates is often high, with the exception of some nodes deep in the tree. If change is frequent then reconstructions are highly uncertain, especially of distant ancestors. Ancestor states for continuous traits are typically highly uncertain. We conclude that measures of uncertainty are useful and should always be provided, despite simplistic assumptions about the probabilistic models that underlie them. If uncertainty is too high, reconstruction should be abandoned in favor of approaches that fit different models of trait evolution to species data and phylogenetic trees, taking into account the range of ancestor states permitted by the data.
2.Mooers, AO; Moller, AP. (1996) Colonial breeding and speciation in birds.Evolutionary Ecology 10: 375-385 Colonial breeding and speciation in birds
aves; coloniality; speciation; diversity
It was recently suggested that bird species which breed colonially might be under stronger sexual selection, have faster rates of evolution and might therefore speciate more rapidly than bird species which do not. If true, then colonial taxa should contain more species than non-colonial taxa, other things being equal. When similarity through common descent is accounted for, there is little evidence for an association between the number of species in a clade and whether it is colonial or not.
