11. Wilson, K; Grzywacz, D; Cory, JS; Donkersley, P; Graham, RI. (2021) Trans-generational viral transmission and immune priming are dose-dependent.J. Anim. Ecol. 90: 1560-1569 Trans-generational viral transmission and immune priming are dose-dependent
baculovirus; immune priming; outbreak pest; vertical transmission; virus triggering
It is becoming increasingly apparent that trans-generational immune priming (i.e. the transfer of the parental immunological experience to its progeny resulting in offspring protection from pathogens that persist across generations) is a common phenomenon not only in vertebrates, but also invertebrates. Likewise, it is known that covert pathogenic infections may become 'triggered' into an overt infection by various stimuli, including exposure to heterologous infections. Yet, rarely have both phenomena been explored in parallel. Using as a model system the African armyworm Spodoptera exempta, an eruptive agricultural pest and its endemic dsDNA virus (Spodoptera exempta nucleopolyhedrovirus, SpexNPV), the aim of this study was to explore the impact of parental inoculating-dose on trans-generational pathogen transmission and immune priming (in its broadest sense). Larvae were orally challenged with one of five doses of SpexNPV and survivors from these treatments were mated and their offspring monitored for viral mortality. Offspring from parents challenged with low viral doses showed evidence of 'immune priming' (i.e. enhanced survival following SpexNPV challenge); in contrast, offspring from parents challenged with higher viral doses exhibited greater susceptibility to viral challenge. Most offspring larvae died of the virus they were orally challenged with; in contrast, most offspring from parents that had been challenged with the highest doses were killed by the vertically transmitted virus (90%) and not the challenge virus. These results demonstrate that the outcome of a potentially lethal virus challenge is critically dependent on the level of exposure to virus in the parental generation-either increasing resistance at very low parental viral doses (consistent with trans-generational immune priming) or increasing susceptibility at higher parental doses (consistent with virus triggering). We discuss the implications of these findings for understanding both natural epizootics of baculoviruses and for using them as biological control agents. DOI PubMed
10. Escasa, SR; Harrison, RL; Mowery, JD; Bauchan, GR; Cory, JS. (2019) The complete genome sequence of an alphabaculovirus from Spodoptera exempta, an agricultural pest of major economic significance in Africa.PLoS One 14 The complete genome sequence of an alphabaculovirus from Spodoptera exempta, an agricultural pest of major economic significance in Africa
Spodoptera exempta nucleopolyhedrovirus (SpexNPV) is a viral pathogen of the African armyworm, Spodoptera exempta (Lepidoptera: Noctuidae), a significant agricultural pest of cereal crops in Africa. SpexNPV has been evaluated as a potential insecticide for control of this pest and has served as the subject of research on baculovirus pathology and transmission. Occlusion bodies (OBs) of SpexNPV isolate 244.1 were examined, and the nucleotide sequence of the genome was determined and characterized. SpexNPV-244.1 OBs consisted of irregular polyhedra with a size and appearance typical for alphabaculoviruses. Virions within the polyhedra contained 1-8 nucleocapsids per unit envelope. The SpexNPV-244.1 genome was comprised of a 129,528 bp circular sequence, in which 139 ORFs were annotated. Five homologous regions (hrs) consisting of a variable number of 28-bp imperfect palindromes were identified in the genome. The genome sequence contained the 38 core genes of family Baculoviridae, as well as three ORFs unique to the SpexNPV sequence and one ORF that was apparently acquired by horizontal gene transfer with a betabaculovirus ancestor. Phylogenetic inference with core gene amino acid sequence alignments placed SpexNPV-244.1 in a lineage containing alphabaculoviruses of Spodoptera frugiperda and Spodopotera exigua which in turn is part of a larger group of alphabaculoviruses from the subfamily Noctuinae in the lepidopteran family Noctuidae. Kimura-2-parameter pairwise nucleotide distances indicated that SpexNPV-244.1 represented a different and previously unlisted species in the genus Alphabaculovirus. Gene parity plots indicated that the gene order of SpexNPV-244. I was extensively collinear with that of Spodoptera exigua NPV (SeMNPV). These plots also revealed a group of 17 core genes whose order was conserved in other alpha-and betabaculoviruses. DOI PubMed
9. Myers, JH; Cory, JS. (2016) Ecology and evolution of pathogens in natural populations of Lepidoptera.Evolutionary Applications 9: 231-247 Ecology and evolution of pathogens in natural populations of Lepidoptera
disease ecology; disease transmission; forest Lepidoptera; insect pathogens; migration; population regulation; tritrophic interactions; virulence
Pathogens are ubiquitous in insect populations and yet few studies examine their dynamics and impacts on host populations. We discuss four lepidopteran systems and explore their contributions to disease ecology and evolution. More specifically, we elucidate the role of pathogens in insect population dynamics. For three species, western tent caterpillars, African armyworm and introduced populations of gypsy moth, infection by nucleopolyhedrovirus (NPV) clearly regulates host populations or reduces their outbreaks. Transmission of NPV is largely horizontal although low levels of vertical transmission occur, and high levels of covert infection in some cases suggest that the virus can persist in a nonsymptomatic form. The prevalence of a mostly vertically transmitted protozoan parasite, Ophryocystis elektroscirrha, in monarch butterflies is intimately related to their migratory behaviour that culls highly infected individuals. Virulence and transmission are positively related among genotypes of this parasite. These systems clearly demonstrate that the interactions between insects and pathogens are highly context dependent. Not only is the outcome a consequence of changes in density and genetic diversity: environmental factors, particularly diet, can have strong impacts on virulence, transmission and host resistance or tolerance. What maintains the high level of host and pathogen diversity in these systems, however, remains a question. DOI
8. Redman, EM; Wilson, K; Cory, JS. (2016) Trade-offs and mixed infections in an obligate-killing insect pathogen.Journal of Animal Ecology 85: 1200-1209 Trade-offs and mixed infections in an obligate-killing insect pathogen
dose-response; entomopathogen; infection diversity; mortality rate; polymorphism; transmission potential; virulence
1. Natural populations of pathogens are frequently composed of numerous interacting strains. Understanding what maintains this diversity remains a key focus of research in disease ecology. In addition, within-host pathogen dynamics can have a strong impact on both infection outcome and the evolution of pathogen virulence, and thus, understanding the impact of pathogen diversity is important for disease management. 2. We compared eight genetically distinguishable variants from Spodoptera exempta nucleopolyhedrovirus (SpexNPV) isolated from the African armyworm, Spodoptera exempta. NPVs are obligate killers, and the vast majority of transmission stages are not released until after the host has died. 3. The NPV variants differed significantly in their virulence and could be clustered into two groups based on their dose-response curves. They also differed in their speed of kill and productivity (transmission potential) for S. exempta. The mixed-genotype wild-type (WT) SpexNPV, from which each variant was isolated, was significantly more virulent than any individual variant and its mean mortality rate was within the fastest group of individual variants. However, the WT virus produced fewer new infectious stages than any single variant, which might reflect competition among the variants. 4. A survival analysis, combining the mortality and speed of kill data, confirmed the superiority of the genetically mixed WT virus over any single variant. Spodoptera exempta larvae infected with WT SpexNPV were predicted to die 2.7 and 1.9 times faster than insects infected with isolates from either of the two clusters of genotypes. 5. Theory suggests that there are likely to be trade-offs between pathogen fitness traits. Across all larvae, there was a negative linear relationship between virus yield and speed of kill, such that more rapid host death carried the cost of producing fewer transmission stages. We also found a near-significant relationship for the same trend at the intervariant level. However, there was no evidence for a significant relationship between the induced level of mortality and transmission potential (virus yield) or speed of kill. DOI
7. Shikano, I; Oak, MC; Halpert-Scanderbeg, O; Cory, JS. (2015) Trade-offs between transgenerational transfer of nutritional stress tolerance and immune priming.Functional Ecology 29: 1156-1164 Trade-offs between transgenerational transfer of nutritional stress tolerance and immune priming
Bacillus thuringiensis; baculovirus; environmental context; fitness costs; food quality; host-parasite interaction; invertebrate immunity; maternal effect; pathogen resistance
Transgenerational effects are often assumed to have adaptive value as a driver of variation in offspring and parental fitness. Studies of transgenerational effects often focus on single environmental variables. However, in nature, it is unlikely for one factor to vary independently from others and there are likely to be trade-offs between different stressors. We altered the nutritional environment of both parents and offspring to examine how nutritional stress influences transgenerational immune priming (TGIP) with a sublethal challenge by the bacterial pathogen Bacillus thuringiensis, in the cabbage looper, Trichoplusia ni. Transgenerational immune priming was adaptive when offspring encountered the same pathogen experienced by their parents, such that offspring resistance to B.thuringiensis increased 15-fold and antibacterial activity in the haemolymph increased by as much as 4-fold. However, this was not a general increase in pathogen resistance as susceptibility to a second pathogen, the baculovirus, TnSNPV remained the same. Interestingly, nutritional stress in the parents both enhanced nutritional stress tolerance of offspring and heightened resistance to both B.thuringiensis and TnSNPV. Elevated pathogen resistance was linked to increased egg size. There was a significant trade-off between TGIP and the transfer of nutritional stress tolerance when parents encountered both stressors simultaneously, such that parents transferred resistance to pathogens but not nutritional stress tolerance. These results highlight the trade-offs that can modulate the occurrence and magnitude of transgenerational effects and illustrate the importance of assessing interactions between multiple environmental variables. At high population densities, disease risk increases and resour-ces become depleted. Thus, our findings could have significant implications for population dynamics. DOI
6. Keever, CC; Nieman, C; Ramsay, L; Ritland, CE; Bauer, LS; Lyons, DB; Cory, JS. (2013) Microsatellite population genetics of the emerald ash borer (Agrilus planipennis Fairmaire): comparisons between Asian and North American populations.Biological Invasions 15: 1537-1559 Microsatellite population genetics of the emerald ash borer (Agrilus planipennis Fairmaire): comparisons between Asian and North American populations
COLEOPTERA BUPRESTIDAE; NATURAL ENEMIES; BIOLOGY; DIFFERENTIATION; DIVERSITY; EVOLUTION; VARIANCE; SOFTWARE; CHINA; PHYLOGEOGRAPHY
The emerald ash borer (EAB) (Agrilus planipennis Fairmaire) (Coleoptera; Buprestidae), is an invasive wood-boring beetle native to northeast Asia. This species was first detected in Michigan USA in 2002, and is a significant threat to native and ornamental ash tree species (Fraxinus spp.) throughout North America. We characterized seven polymorphic microsatellite markers for EAB and used these to investigate EAB population structure in the early invasive populations within North America and in comparison with Asia. We found 2-9 alleles per microsatellite locus, no evidence of linkage disequilibrium, and no association with known coding sequences, suggesting that these markers are suitable for population genetic analysis. Microsatellite population genetic structure was examined in 48 EAB populations sampled between 2003 and 2008 from five regions, three in the introduced range, Michigan (US) and Ontario and Quebec (Canada) and two Asian regions, China and South Korea, where EAB is native. We found significant genetic variation geographically but not temporally in EAB populations. Bayesian clustering analyses of individual microsatellite genotypes showed strong clustering among multiple North American populations and populations in both China and South Korea. Finally, allelic richness and expected heterozygosity were higher in the native range of EAB, but there was no difference in observed heterozygosity, suggesting a significant loss of alleles upon introduction but no significant change in the distribution of alleles within and among individuals. DOI
5.Cory, JS; Hoover, K. (2006) Plant-mediated effects in insect-pathogen interactions.Trends in Ecology & Evolution 21: 278-286 Plant-mediated effects in insect-pathogen interactions
Interactions between insect herbivores and their pathogens can be modulated by host plants. Inter- and intraspecific differences in plant chemistry and structure can after the susceptibility of insects to infection and the production and environmental persistence of pathogens. Whether plants can manipulate insect pathogens to act as 'bodyguards' and increase their own fitness remains to be shown. Reduced insect performance owing to poor plant quality can enhance the susceptibility of an insect to disease while these same phytochemicals can also reduce the effectiveness of entomopathogens in killing the host. As we discuss here, plants have an important role in the evolution of insect-pathogen relationships and a tritrophic perspective should thus be incorporated into the study of insects and their pathogens. DOI
4.Cory, JS; Myers, JH. (2003) The ecology and evolution of insect baculoviruses.Annual Review of Ecology Evolution and Systematics 34: 239-272 The ecology and evolution of insect baculoviruses
virulence; resistance; pathogen; variation; transmission
Baculoviruses occur widely among Lepidoptera, and in some species of forest and agricultural insects, they cause epizootics in outbreak populations. Here we review recent developments in baculovirus ecology and evolution, in particular focusing on emerging areas of interest and studies relating to field populations. The expanding application of molecular techniques has started to reveal the structure of baculovirus populations and has highlighted how variable these pathogens are both genotypically and phenotypically at all levels from within individual hosts to among host populations. In addition, the detailed molecular knowledge available for baculoviruses has allowed the interpretation of gene functions across physiological and population levels in a way rarely possible in parasite-host systems and showed the diverse mechanisms that these viruses use to exploit their hosts. Analysis of the dynamic interactions between insects and baculoviruses, and their compatibility for laboratory and field experiments, has formed a basis for studies that have made a significant contribution to unraveling disease interactions in insect populations. In particular, manipulative studies on baculoviruses have been instrumental in developing an understanding of disease transmission dynamics. The results so far indicate that baculoviruses have the potential to be an excellent model for investigations of changes in virulence and resistance in fluctuating and stable host populations. DOI
3. Herniou, EA; Olszewski, JA; Cory, JS; O'Reilly, DR. (2003) The genome sequence and evolution of baculoviruses.Annual Review of Entomology 48: 211-234 The genome sequence and evolution of baculoviruses
Baculoviridae; phylogeny; gene order; gene composition; gene function
Comparative analysis of the complete genome sequences of 13 baculoviruses revealed a core set of 30 genes, 20 of which have known functions. Phylogenetic analyses of these 30 genes yielded a tree with 4 major groups: the genus Granulovirus (GVs), the group I and II lepidopteran nucleopolyhedroviruses (NPVs), and the dipteran NPV, CuniNPV. These major divisions within the family Baculoviridae were also supported by phylogenies based on gene content and gene order. Gene content mapping has revealed the patterns of gene acquisitions and losses that have taken place during baculovirus evolution, and it has highlighted the fluid nature of baculovirus genomes. The identification of shared protein phylogenetic profiles provided evidence for two putative DNA repair systems and for viral proteins specific for infection of lymantrid hosts. Examination of gene order conservation revealed a core gene cluster of four genes, helicase, lef-5, ac96, and 38K(ac98), whose relative positions are conserved in all baculovirus genomes. DOI
1. CORY, JS; HIRST, ML; WILLIAMS, T; HAILS, RS; GOULSON, D; GREEN, BM; CARTY, TM; POSSEE, RD; CAYLEY, PJ; BISHOP, DHL. (1994) FIELD TRIAL OF A GENETICALLY IMPROVED BACULOVIRUS INSECTICIDE.Nature 370: 138-140 FIELD TRIAL OF A GENETICALLY IMPROVED BACULOVIRUS INSECTICIDE
IMPROVEMENT of biological pesticides through genetic modification has enormous potential and the insect baculoviruses are particularly amenable to this approach(1,2). A key aim of genetic engineering is to increase their speed of kill, primarily by the incorporation of genes which encode arthropod or bacterially derived insect-selective toxins(3-11), insect hormones(12,13) or enzymes(14,15). We report here the first, to our knowledge, field trial of a genetically improved nuclear polyhedrosis virus of the alfalfa looper, Autographa californica (AcNPV) that expresses an insect-selective toxin gene (AaHIT) derived from the venom of the scorpion Androctonus australis(16-18). Previous laboratory assays with the cabbage looper, Trichoplusia ni, demonstrated a 25% reduction in time to death compared to the wild-type virus, but unaltered pathogenicity(6) and host range(19). In the field, the modified baculovirus killed faster, resulting in reduced crop damage and it appeared to reduce the secondary cycle of infection compared to the wild-type virus.
