Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-23T04:02:39.892Z Has data issue: false hasContentIssue false

The recurrent domestication of viruses: major evolutionary transitions in parasitic wasps

Published online by Cambridge University Press:  23 May 2017

Jérémy Gauthier
Affiliation:
Institut de Recherche sur la Biologie de l'Insecte, CNRS UMR 7261, Université François-Rabelais de Tours, UFR Sciences et Techniques, 37200 Tours, France
Jean-Michel Drezen
Affiliation:
Institut de Recherche sur la Biologie de l'Insecte, CNRS UMR 7261, Université François-Rabelais de Tours, UFR Sciences et Techniques, 37200 Tours, France
Elisabeth A. Herniou*
Affiliation:
Institut de Recherche sur la Biologie de l'Insecte, CNRS UMR 7261, Université François-Rabelais de Tours, UFR Sciences et Techniques, 37200 Tours, France
*
Author for correspondence: E. Herniou, E-mail: [email protected]

Abstract

Several lineages of endoparasitoid wasps, which develop inside the body of other insects, have domesticated viruses, used as delivery tools of essential virulence factors for the successful development of their progeny. Virus domestications are major evolutionary transitions in highly diverse parasitoid wasps. Much progress has recently been made to characterize the nature of these ancestrally captured endogenous viruses that have evolved within the wasp genomes. Virus domestication from different viral families occurred at least three times in parasitoid wasps. This evolutionary convergence led to different strategies. Polydnaviruses (PDVs) are viral gene transfer agents and virus-like particles of the wasp Venturia canescens deliver proteins. Here, we take the standpoint of parasitoid wasps to review current knowledge on virus domestications by different parasitoid lineages. Then, based on genomic data from parasitoid wasps, PDVs and exogenous viruses, we discuss the different evolutionary steps required to transform viruses into vehicles for the delivery of the virulence molecules that we observe today. Finally, we discuss how endoparasitoid wasps manipulate host physiology and ensure parasitism success, to highlight the possible advantages of viral domestication as compared with other virulence strategies.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

These authors contributed equally to this work.

References

Abergel, C, Legendre, M and Claverie, J-M (2015) The rapidly expanding universe of giant viruses: Mimivirus, Pandoravirus, Pithovirus and Mollivirus. Federation of European Microbiology Societies Microbiological Reviews 39, 779796. doi: 10.1093/femsre/fuv037Google ScholarPubMed
Agra Gothama, AA, Sikorowski, PP and McLaughlin, MR (1998) Replication of nonoccluded baculovirus associated with the parasitoid Microplitis croceipes (Hymenoptera: Braconidae) in Heliothis virescens (Lepidoptera: Noctuidae). Biological Control 12, 103110. doi: 10.1006/bcon.1998.0575.Google Scholar
Andrew, N, Basio, M and Kim, Y (2006) Additive effect of teratocyte and calyx fluid from Cotesia plutellae on immunosuppression of Plutella xylostella. Physiological Entomology 31, 341347. doi: 10.1111/j.1365-3032.2006.00524.x.Google Scholar
Asgari, S, et al. (2003) Isolation and characterization of a novel venom protein from an endoparasitoid, Cotesia rubecula (Hym: Braconidae). Archives of Insect Biochemistry and Physiology 53, 92100. doi: 10.1002/arch.10088.Google Scholar
Barratt, BIP, et al. (1999) Virus-like particles in the ovaries of Microctonus aethiopoides loan (Hymenoptera: Braconidae), a parasitoid of adult weevils (Coleoptera: Curculionidae). Journal of Invertebrate Pathology 73, 182188. doi: 10.1006/jipa.1998.4826.CrossRefGoogle ScholarPubMed
Beck, MH, Inman, RB and Strand, MR (2007) Microplitis demolitor bracovirus genome segments vary in abundance and are individually packaged in virions. Virology 359, 179189. doi: 10.1016/j.virol.2006.09.002.Google Scholar
Beck, MH, et al. (2011) The encapsidated genome of Microplitis demolitor bracovirus integrates into the host Pseudoplusia includens. Journal of Virology 85, 1168511696. doi: 10.1128/JVI.05726-11.Google Scholar
Beckage, NE (1998) Modulation of immune responses to parasitoids by polydnaviruses. Parasitology 116(Suppl.), S57S64. doi: 10.1017/S0031182000084948.Google Scholar
Beckage, NE (2012) Polydnaviruses as endocrine regulators. In Beckage, NE and Drezen, J-M (ed.), Parasitoid Viruses. San Diego, USA: Academic Press, pp. 163168. doi: 10.1016/B978-0-12-384858-1.00013-8.Google Scholar
Beckage, NE and Buron, ID (1997) Developmental changes in teratocytes of the braconid wasp Cotesia congregata in larvae of the tobacco hornworm, Manduca sexta. Journal of Insect Physiology 43, 915930. doi: 10.1016/S0022-1910(97)00056-5.Google Scholar
Beckage, NE, et al. (1990) Host hemolymph monophenoloxidase activity in parasitized Manduca sexta larvae and evidence for inhibition by wasp polydnavirus. Insect Biochemistry 20, 285294. doi: 10.1016/0020-1790(90)90046-W.Google Scholar
Béliveau, C, et al. (2015) Genomic and proteomic analyses indicate that banchine and campoplegine polydnaviruses have similar, if not identical, viral ancestors. Journal of Virology 89, 89098921. doi: 10.1128/JVI.01001-15.Google Scholar
Bézier, A, et al. (2008) Bracovirus gene products are highly divergent from insect proteins. Archives of Insect Biochemistry and Physiology 67, 172187. doi: 10.1002/arch.20219.Google Scholar
Bézier, A, et al. (2009 a). Polydnaviruses of braconid wasps derive from an ancestral nudivirus. Science 323, 926930. doi: 10.1126/science.1166788.Google Scholar
Bézier, A, et al. (2016) Qualitative proteomic analysis of Tipula oleracea nudivirus (ToNV) occlusion bodies. Journal of General Virology 98, 284295. doi: 10.1099/jgv.0.000661.CrossRefGoogle Scholar
Bézier, A, et al. (2009 b). Polydnavirus hidden face: the genes producing virus particles of parasitic wasps. Journal of Invertebrate Pathology 101, 194203. doi: 10.1016/j.jip.2009.04.006.Google Scholar
Bézier, A, et al. (2013) Functional endogenous viral elements in the genome of the parasitoid wasp Cotesia congregata: insights into the evolutionary dynamics of bracoviruses. Philosophical Transactions of the Royal Society B: Biological Sciences 368, 2013004720130047. doi: 10.1186/1741-7007-6-38.Google Scholar
Bézier, A, et al. (2015) The genome of the nucleopolyhedrosis-causing virus from Tipula oleracea sheds new light on the Nudiviridae family. Journal of Virology 89, 30083025. doi: 10.1128/JVI.02884-14.CrossRefGoogle ScholarPubMed
Bigler, F, Babendreier, D and Kuhlmann, U (2006) Environmental Impact of Invertebrates for Biological Control of Arthropods: Methods and Risk Assessment. Wallingford, UK: CABI Publishing.Google Scholar
Bigot, Y, et al. (1997) Biological and molecular features of the relationships between Diadromus pulchellus ascovirus, a parasitoid hymenopteran wasp (Diadromus pulchellus) and its lepidopteran host, Acrolepiopsis assectella. Journal of General Virology 78, 11491163. doi: 10.1099/0022-1317-78-5-1149.CrossRefGoogle ScholarPubMed
Burand, JP, et al. (2012) Analysis of the genome of the sexually transmitted insect virus Helicoverpa zea Nudivirus 2. Viruses 4, 2861. doi: 10.3390/v4010028.Google Scholar
Burke, GR and Strand, MR (2012 a). Polydnaviruses of parasitic wasps: domestication of viruses to act as gene delivery vectors. Insects 3, 91119. doi: 10.3390/insects3010091.Google Scholar
Burke, GR and Strand, MR (2012 b). Deep sequencing identifies viral and wasp genes with potential roles in replication of Microplitis demolitor bracovirus. Journal of Virology 86, 32933306. doi: 10.1128/JVI.06434-11.Google Scholar
Burke, GR and Strand, MR (2014) Systematic analysis of a wasp parasitism arsenal. Molecular Ecology 23, 890901. doi: 10.1111/mec.12648.Google Scholar
Burke, GR, et al. (2013) Mutualistic polydnaviruses share essential replication gene functions with pathogenic ancestors. PLoS Pathogens 9, 114. doi: 10.1371/journal.ppat.1003348.Google Scholar
Burke, GR, et al. (2014) Widespread genome reorganization of an obligate virus mutualist. PLoS Genetics 10, e1004660. doi: 10.1371/journal.pgen.1004660.s007.Google Scholar
Burke, GR, et al. (2015) Microplitis demolitor bracovirus proviral loci and clustered replication genes exhibit distinct DNA amplification patterns during replication. Journal of Virology 89, 95119523. doi: 10.1128/JVI.01388-15.Google Scholar
Butcher, BA, et al. (2012) A turbo-taxonomic study of Thai Aleiodes (Aleiodes) and Aleiodes (Arcaleiodes) (Hymenoptera: Braconidae: Rogadinae) based largely on COI barcoded specimens, with rapid descriptions of 179 new species. Zootaxa 3457, 1232.Google Scholar
Cheng, R-L, et al. (2014) Brown planthopper nudivirus DNA integrated in its host genome. Journal of Virology 88, 53105318. doi: 10.1128/JVI.03166-13.Google Scholar
Chevignon, G, et al. (2014) Functional annotation of Cotesia congregata bracovirus: identification of viral genes expressed in parasitized host immune tissues. Journal of Virology 88, 87958812. doi: 10.1128/JVI.00209-14.Google Scholar
Chevignon, G, et al. (2015) Transcriptomic response of Manduca sexta immune tissues to parasitization by the bracovirus associated wasp Cotesia congregata. Insect Biochemistry and Molecular Biology 62, 8699. doi: 10.1016/j.ibmb.2014.12.008.Google Scholar
Dahlman, DL, et al. (2003) A teratocyte gene from a parasitic wasp that is associated with inhibition of insect growth and development inhibits host protein synthesis. Insect Molecular Biology 12, 527534. doi: 10.1046/j.1365-2583.2003.00439.x.Google Scholar
Dani, MP and Richards, EH (2010) Identification, cloning and expression of a second gene (vpr1) from the venom of the endoparasitic wasp, Pimpla hypochondriaca that displays immunosuppressive activity. Journal of Insect Physiology 56, 195203. doi: 10.1016/j.jinsphys.2009.10.006.CrossRefGoogle ScholarPubMed
Dani, MP, et al. (2003) Antibacterial and proteolytic activity in venom from the endoparasitic wasp Pimpla hypochondriaca (Hymenoptera: Ichneumonidae). Journal of Insect Physiology 49, 945954. doi: 10.1016/S0022-1910(03)00163-X.Google Scholar
Desjardins, CA, et al. (2008) Comparative genomics of mutualistic viruses of Glyptapanteles parasitic wasps. Genome Biology 9, 1. doi: 10.1186/gb-2008-9-12-r183.Google Scholar
Digilio, MC, Pennacchio, F and Tremblay, E (1998) Host regulation effects of ovary fluid and venom of Aphidius ervi (Hymenoptera: Braconidae). Journal of Insect Physiology 44, 779784. doi: 10.1016/S0022-1910(98)00010-9.CrossRefGoogle Scholar
Digilio, MC, et al. (2000) Host castration by Aphidius ervi venom proteins. Journal of Insect Physiology 46, 10411050. doi: 10.1016/S0022-1910(99)00216-4.Google Scholar
Doucet, D, et al. (2007) In vitro integration of an ichnovirus genome segment into the genomic DNA of lepidopteran cells. Journal of General Virology 88, 105113. doi: 10.1099/vir.0.82314-0.Google Scholar
Drezen, J-M, et al. (2016) Foreign DNA acquisition by invertebrate genomes. Journal of Invertebrate Pathology. doi: 10.1016/j.jip.2016.09.004.Google Scholar
Du, S and Traktman, P (1996) Vaccinia virus DNA replication: two hundred base pairs of telomeric sequence confer optimal replication efficiency on minichromosome templates. Proceedings of the National Academy of Sciences of the United States of America 93, 96939698.Google Scholar
Dunning Hotopp, JC, et al. (2007) Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317, 17531756. doi: 10.1126/science.1142490.Google Scholar
Dupas, S, et al. (1996) Immune suppressive virus-like particles in a Drosophila parasitoid: significance of their intraspecific morphological variations. Parasitology 113, 207212. doi: 10.1017/S0031182000081981.Google Scholar
Dupas, S, et al. (2008) Evolution of a polydnavirus gene in relation to parasitoid-host species immune resistance. Journal of Heredity 99, 491499. doi: 10.1093/jhered/esn047.Google Scholar
Dupuy, C, Gundersen-Rindal, D and Cusson, M (2012) Genomics and replication of polydnaviruses. In Beckage, NE and Drezen, J-M (ed.), Parasitoid Viruses. San Diego, USA: Academic Press, pp. 4761. doi: 10.1016/B978-0-12-384858-1.00004-7.Google Scholar
Dushay, MS and Beckage, NE (1993) Dose-dependent separation of Cotesia congregata-associated polydnavirus effects on Manduca sexta larval development and immunity. Journal of Insect Physiology 39, 10291040. doi: 10.1016/0022-1910(93)90127-D.Google Scholar
Falabella, P, et al. (2007) Characterization of the IκB-like gene family in polydnaviruses associated with wasps belonging to different braconid subfamilies. Journal of General Virology 88, 92104. doi: 10.1099/vir.0.82306-0.Google Scholar
Gao, F, et al. (2016) Cotesia vestalis teratocytes express a diversity of genes and exhibit novel immune functions in parasitism. Scientific Reports 6, 26967. doi: 10.1038/srep26967.Google Scholar
Gasmi, L, et al. (2015) Recurrent domestication by Lepidoptera of genes from their parasites mediated by bracoviruses. PLoS Genetics 11, e1005470. doi: 10.1371/journal.pgen.1005470.s007.CrossRefGoogle ScholarPubMed
Gauld, ID and Bolton, B (1988) The Hymenoptera. London, UK: Oxford University Press in association with British Museum (Natural History).Google Scholar
Godfray, HCJ (1994) Parasitoids: Behavioral and Evolutionary Ecology. Princeton, NJ, USA: Princeton University Press.CrossRefGoogle Scholar
Hamm, JJ, Styer, EL and Lewis, WJ (1988) A baculovirus pathogenic to the parasitoid Microplitis croceipes (Hymenoptera: Braconidae). Journal of Invertebrate Pathology 52, 189191.Google Scholar
Hawkins, BA (1994) Pattern and Process in Host-Parasitoid Interactions. Cambridge, UK: Cambridge University Press.Google Scholar
Henneman, ML and Memmott, J (2001) Infiltration of a Hawaiian community by introduced biological control agents. Science 293, 13141316. doi: 10.1126/science.1060788.Google Scholar
Henry, LM, Roitberg, BD and Gillespie, DR (2008) Host-range evolution in Aphidius parasitoids: fidelity, virulence and fitness trade-offs on an ancestral host. Evolution 62, 689699. doi: 10.1111/j.1558-5646.2007.00316.x.CrossRefGoogle Scholar
Herniou, EA, et al. (2013) When parasitic wasps hijacked viruses: genomic and functional evolution of polydnaviruses. Philosophical Transactions of the Royal Society of London. Series B. 368, 20130051. doi: 10.1098/rstb.2013.0051.CrossRefGoogle ScholarPubMed
Hoover, K, et al. (2011) A gene for an extended phenotype. Science 333, 1401. doi: 10.1126/science.1209199.Google Scholar
Husnik, F, et al. (2013) Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell 153, 15671578. doi: 10.1016/j.cell.2013.05.040.Google Scholar
Jacas, JA, et al. (1997) Virus-like particles in the poison gland of the parasitic wasp Opius concolor. Annals of Applied Biology 130, 587592. doi: 10.1111/j.1744-7348.1997.tb07685.x.Google Scholar
Jancek, S, et al. (2013) Adaptive selection on bracovirus genomes drives the specialization of Cotesia parasitoid wasps. PLoS ONE 8(5), e64432. doi: 10.1371/journal.pone.0064432.CrossRefGoogle ScholarPubMed
Kadono-Okuda, K, et al. (1995) Synchronous growth of a parasitoid, Perilitus coccinellae, and teratocytes with the development of the host, Coccinella septempunctata. Entomologia Experimentalis et Applicata 75, 145149. doi: 10.1111/j.1570-7458.1995.tb01920.x.CrossRefGoogle Scholar
Kaiser, L, et al. (2015) Ongoing ecological speciation in Cotesia sesamiae, a biological control agent of cereal stem borers. Evolutionary Applications 8, 807–20. doi: 10.1111/eva.12260.Google Scholar
Kariithi, HM, et al. (2010) Proteomic analysis of Glossina pallidipes salivary gland hypertrophy virus virions for immune intervention in tsetse fly colonies. Journal of General Virology 91, 30653074. doi: 10.1099/vir.0.023671-0.Google Scholar
Kim, JC and Orr-Weaver, TL (2011) Analysis of a Drosophila amplicon in follicle cells highlights the diversity of metazoan replication origins. Proceedings of the National Academy of Sciences of the United States of America 108, 1668116686. doi: 10.1073/pnas.1114209108.Google Scholar
Kornberg, A and Baker, TA (2005) DNA replication. Sausalito, CA: University Science.Google Scholar
Kraaijeveld, AR and Van Alphen, JJM (1995) Geographical variation in encapsulation ability of Drosophila melanogaster larvae and evidence for parasitoid-specific components. Evolutionary Ecology 9, 1017. doi: 10.1007/BF01237692.Google Scholar
Lavialle, C, et al. (2013) Paleovirology of ‘syncytins’, retroviral env genes exapted for a role in placentation. Philosophical Transactions of the Royal Society B: Biological Sciences 368, 20120507. doi: 10.1186/1742-4690-2-19.Google Scholar
Leclercq, S, et al. (2016) Birth of a W sex chromosome by horizontal transfer of Wolbachia bacterial symbiont genome. Proceedings of the National Academy of Sciences of the United States of America 113, 15036–15041. doi: 10.1073/pnas.1608979113.Google Scholar
Lin, CL, et al. (1999) Persistent Hz-1 virus infection in insect cells: evidence for insertion of viral DNA into host chromosomes and viral infection in a latent status. Journal of Virology 73, 128139.Google Scholar
Login, FH, et al. (2011) Antimicrobial peptides keep insect endosymbionts under control. Science 334, 362365. doi: 10.1126/science.1209728.Google Scholar
Louis, F, et al. (2013) The bracovirus genome of the parasitoid wasp Cotesia congregata is amplified within 13 replication units, including sequences not packaged in the particles. Journal of Virology 87, 96499660. doi: 10.1128/JVI.00886-13.Google Scholar
Masson, F, et al. (2015) Weevil endosymbiont dynamics is associated with a clamping of immunity. BMC Genomics 16, 819. doi: 10.1186/s12864-015-2048-5.Google Scholar
Moran, NA (2007) Symbiosis as an adaptive process and source of phenotypic complexity. Proceedings of the National Academy of Sciences of the United States of America 104, 86278633. doi: 10.1073/pnas.0611659104.Google Scholar
Moreau, SJM (2013) ‘It stings a bit but it cleans well’: venoms of Hymenoptera and their antimicrobial potential. Journal of Insect Physiology 59, 186204. doi: 10.1016/j.jinsphys.2012.10.005.Google Scholar
Moreau, SJM and Asgari, S (2015) Venom proteins from parasitoid wasps and their biological functions. Toxins 7, 23852412. doi: 10.3390/toxins7072385.Google Scholar
Moreau, SJM, et al. (2002) Effects of parasitism by Asobara tabida (Hymenoptera: Braconidae) on the development, survival and activity of Drosophila melanogaster larvae. Journal of Insect Physiology 48, 337347. doi: 10.1016/S0022-1910(02)00051-3.Google Scholar
Muirhead, KA, et al. (2012) Phylogenetics and genetic diversity of the Cotesia flavipes complex of parasitoid wasps (Hymenoptera: Braconidae), biological control agents of lepidopteran stemborers. Molecular Phylogenetics and Evolution 63, 904914. doi: 10.1016/j.ympev.2012.03.003.Google Scholar
Murphy, N, et al. (2008) Phylogeny of the parasitic microgastroid subfamilies (Hymenoptera: Braconidae) based on sequence data from seven genes, with an improved time estimate of the origin of the lineage. Molecular Phylogenetics and Evolution 47, 378395. doi: 10.1016/j.ympev.2008.01.022.Google Scholar
Nakamatsu, Y, Fujii, S and Tanaka, T (2002) Larvae of an endoparasitoid, Cotesia kariyai (Hymenoptera: Braconidae), feed on the host fat body directly in the second stadium with the help of teratocytes. Journal of Insect Physiology 48, 10411052. doi: 10.1016/S0022-1910(02)00192-0.Google Scholar
Osman, SE (1974) Parasitentoleranz von schmetterlingspuppen maskierung der parasiteneier mit mucopolysacchariden. Naturwissenschaften 61, 453454.Google Scholar
Pasquier-Barre, F, et al. (2002) Polydnavirus replication: the EP1 segment of the parasitoid wasp Cotesia congregata is amplified within a larger precursor molecule. Journal of General Virology 83, 20352045. doi: 10.1099/0022-1317-83-8-2035.Google Scholar
Peng, K, et al. (2010) Baculovirus per os infectivity factors form a complex on the surface of occlusion-derived virus. Journal of Virology 84, 94979504. doi: 10.1128/JVI.00812-10.CrossRefGoogle Scholar
Pennacchio, F and Strand, MR (2006) Evolution of developmental strategies in parasitic Hymenoptera. Annual Review of Entomology 51, 233258. doi: 10.1146/annurev.ento.51.110104.151029.Google Scholar
Pichon, A, et al. (2015) Recurrent DNA virus domestication leading to different parasite virulence strategies. Science Advances 1, e1501150e1501150. doi: 10.1126/sciadv.1501150.CrossRefGoogle ScholarPubMed
Piek, T (1990) Neurotoxins from venoms of the Hymenoptera – twenty-five years of research in Amsterdam. Comparative Biochemistry and Physiology. C: Comparative Pharmacology and Toxicology 96, 223233. doi: 10.1016/0742-8413(90)90001-P.Google Scholar
Provost, B, et al. (2004) Bracoviruses contain a large multigene family coding for protein tyrosine phosphatases. Journal of Virology 78, 1309013103. doi: 10.1128/JVI.78.23.13090-13103.2004.Google Scholar
Quicke, DLJ (2015) The Braconid and Ichneumonid Parasitoid Wasps: Biology, Systematics, Evolution and Ecology. Oxford, UK: Wiley-Blackwell.Google Scholar
Raina, AK, et al. (2000) Further characterization of the gonad-specific virus of corn earworm, Helicoverpa zea. Journal of Invertebrate Pathology 76, 612. doi: 10.1006/jipa.2000.4942.Google Scholar
Rodriguez, JJ, et al. (2013) Extrapolations from field studies and known faunas converge on dramatically increased estimates of global microgastrine parasitoid wasp species richness (Hymenoptera: Braconidae). Insect Conservation and Diversity 6, 530536. doi: 10.1111/icad.12003.CrossRefGoogle Scholar
Rohrmann, G. F (2013) Baculovirus Molecular Biology, 3rd Edn. National Center for Biotechnology Information, Bethesda, USA.Google ScholarPubMed
Ros, VID, et al. (2015) Baculovirus-induced tree-top disease: how extended is the role of egt as a gene for the extended phenotype? Molecular Ecology 24, 249258. doi: 10.1111/mec.13019.Google Scholar
Rotheram, S (1967) Immune surface of eggs of a parasitic insect. Nature 214, 700. doi: 10.1038/214700a0.CrossRefGoogle ScholarPubMed
Savary, S, et al. (1997) Excision of the polydnavirus chromosomal integrated EP1 sequence of the parasitoid wasp Cotesia congregata (Braconidae, Microgastrinae) at potential recombinase binding sites. Journal of General Virology 78, 31253134. doi: 10.1099/0022-1317-78-12-3125.Google Scholar
Savary, S, et al. (1999) The excision of polydnavirus sequences from the genome of the wasp Cotesia congregata (Braconidae, Microgastrinae) is developmentally regulated but not strictly restricted to the ovaries in the adult. Insect Molecular Biology 8, 319327. doi: 10.1046/j.1365-2583.1999.83130.x.Google Scholar
Serbielle, C, et al. (2008) Viral cystatin evolution and three-dimensional structure modelling: a case of directional selection acting on a viral protein involved in a host-parasitoid interaction. BMC Biology 6, 38. doi: 10.1186/1741-7007-6-38.Google Scholar
Serbielle, C, et al. (2009) Identification of parasite-responsive cysteine proteases in Manduca sexta. Biological Chemistry 390, 493502. doi: 10.1515/BC.2009.061.Google Scholar
Serbielle, C, et al. (2012) Evolutionary mechanisms driving the evolution of a large polydnavirus gene family coding for protein tyrosine phosphatases. BMC Evolutionary Biology 12, 253. doi: 10.1186/1471-2148-12-253.Google Scholar
Shaw, MR and Quicke, DLJ (2000) The biology and early stages of Acampsis alternipes (Nees), with comments on the relationships of the Sigalphinae (Hymenoptera: Braconidae). Journal of Natural History 34, 611628. doi: 10.1080/002229300299471.CrossRefGoogle Scholar
Smith, AM, et al. (2013) DNA barcoding and the taxonomy of Microgastrinae wasps (Hymenoptera, Braconidae): impacts after 8 years and nearly 20 000 sequences. Molecular Ecology Resources 13, 168–76. doi: 10.1111/1755-0998.12038.Google Scholar
Stoltz, DB and Cook, DI (1983) Inhibition of host phenoloxidase activity by parasitoid hymenoptera. Experientia 39, 10221024. doi: 10.1007/BF01989783.Google Scholar
Stoltz, DB and Krell, P (2012) The Origins and Early History of Polydnavirus Research. In Beckage, NE and Drezen, J-M (ed.), Parasitoid Viruses: Symbionts and Pathogens. London, UK: Academic Press, pp. 513.Google Scholar
Stoltz, DB and Vinson, SB (1979) Viruses and parasitism in insects. Advances in Virus Research 24, 125–71.Google Scholar
Stoltz, DB and Whitfield, JB (2009) Making nice with viruses. Science 323, 884885. doi: 10.1126/science.1169808.Google Scholar
Strand, MR and Burke, GR (2014) Polydnaviruses: nature's genetic engineers. Annual Review of Virology 1, 333354. doi: 10.1146/annurev-virology-031413-085451.Google Scholar
Strand, MR and Dover, BA (1991) Developmental disruption of Pseudoplusia includens and Heliothis virescens larvae by the calyx fluid and venom of Microplitis demolitor. Archives of Insect Biochemistry and Physiology 18, 131145. doi: 10.1002/arch.940180302.Google Scholar
Strand, MR and Wong, EA (1991) The growth and role of Microplitis demolitor teratocytes in parasitism of Pseudoplusia includens. Journal of Insect Physiology 37, 503515. doi: 10.1016/0022-1910(91)90027-W.Google Scholar
Suzuki, M and Tanaka, T (2006) Virus-like particles in venom of Meteorus pulchricornis induce host hemocyte apoptosis. Journal of Insect Physiology 52, 602613. doi: 10.1016/j.jinsphys.2006.02.009.Google Scholar
Tanaka, T (1987) Calyx and venom fluids of Apanteles kariyai (Hymenoptera: Braconidae) as factors that prolong larval period of the host, Pseudaletia separata (Lepidoptera: Noctuidae). Annals of the Entomological Society of America 80, 530533. doi: 10.1093/aesa/80.4.530.Google Scholar
Tanaka, T and Wago, H (1990) Ultrastructural and functional maturation of teratocytes of Apanteles kariyai. Archives of Insect Biochemistry and Physiology 13, 187197. doi: 10.1002/arch.940130306.Google Scholar
Thézé, J, et al. (2011) Paleozoic origin of insect large dsDNA viruses. Proceedings of the National Academy of Sciences of the United States of America 108, 1593115935. doi: 10.1073/pnas.1105580108.Google Scholar
van Houte, S, Ros, VID and van Oers, MM (2014) Hyperactivity and tree-top disease induced by the baculovirus AcMNPV in Spodoptera exigua larvae are governed by independent mechanisms. Die Naturwissenschaften 101, 347350. doi: 10.1007/s00114-014-1160-8.Google Scholar
van Rij, RP and Berezikov, E (2009) Small RNAs and the control of transposons and viruses in Drosophila. Trends in Microbiology 17, 163171. doi: 10.1016/j.tim.2009.01.003.Google Scholar
van Valen, L (1973) A new evolutionary law. Evolutionary Theory 1, 1–30.Google Scholar
Vincent, B, et al. (2010) The venom composition of the parasitic wasp Chelonus inanitus resolved by combined expressed sequence tags analysis and proteomic approach. BMC Genomics 11, 693. doi: 10.1186/1471-2164-11-693.Google Scholar
Volkoff, A-N, et al. (2010) Analysis of virion structural components reveals vestiges of the ancestral ichnovirus genome. PLoS Pathogens 6, 110. doi: 10.1371/journal.ppat.1000923.Google Scholar
Volkoff, A-N, et al. (2012) The organization of genes encoding ichnovirus structural proteins. In Beckage, NE and Drezen, J-M (ed.), Parasitoid Viruses. San Diego, USA: Academic Press, pp. 3345. doi: 10.1016/B978-0-12-384858-1.00003-5.Google Scholar
Wang, J and Aksoy, S (2012) PGRP-LB is a maternally transmitted immune milk protein that influences symbiosis and parasitism in tsetse's offspring. Proceedings of the National Academy of Sciences of the United States of America 109, 1055210557. doi: 10.1073/pnas.1116431109.CrossRefGoogle ScholarPubMed
Wang, Y, Burand, JP and Jehle, JA (2007 a). Nudivirus genomics: diversity and classification. Virologica Sinica 22, 128136. doi: 10.1007/s12250-007-0014-3.Google Scholar
Wang, Y, et al. (2007 b). The genome of Gryllus bimaculatus nudivirus indicates an ancient diversification of baculovirus-related nonoccluded nudiviruses of insects. Journal of Virology 81, 53955406. doi: 10.1128/JVI.02781-06.Google Scholar
Wang, Y, et al. (2011) The genome of Oryctes rhinoceros nudivirus provides novel insight into the evolution of nuclear arthropod-specific large circular double-stranded DNA viruses. Virus Genes 42, 444456. doi: 10.1007/s11262-011-0589-5.Google Scholar
Wang, Y, Bininda-Emonds, ORP and Jehle, JA (2012) Nudivirus genomics and phylogeny. In Garcia, M. L and Romanowski, V (ed.), The Viral Genome: Molecular Structure, Diversity, Gene Expression Mechanisms and Host-Virus Interactions. InTech, Rijeka, Croatia, pp. 33–52.Google Scholar
Weber, B, Annaheim, M and Lanzrein, B (2007) Transcriptional analysis of polydnaviral genes in the course of parasitization reveals segment-specific patterns. Archives of Insect Biochemistry and Physiology 66, 922. doi: 10.1002/arch.20190.Google Scholar
Weller, SK and Coen, DM (2012) Herpes simplex viruses: mechanisms of DNA replication. Cold Spring Harbor Perspectives in Biology 4, a013011. doi: 10.1101/cshperspect.a013011.Google Scholar
Wetterwald, C, et al. (2010) Identification of bracovirus particle proteins and analysis of their transcript levels at the stage of virion formation. Journal of General Virology 91, 26102619. doi: 10.1099/vir.0.022699-0.Google Scholar
Whitfield, JB (2002) Estimating the age of the polydnavirus/braconid wasp symbiosis. Proceedings of the National Academy of Sciences of the United States of America 99, 75087513. doi: 10.1073/pnas.112067199.CrossRefGoogle ScholarPubMed
Whitfield, JB and O’Connor, JM (2012) Molecular systematics of wasp and polydnavirus genomes and their coevolution. In Beckage, NE and Drezen, J-M (ed.), Parasitoid Viruses. San Diego, USA: Academic Press, pp. 8997. doi: 10.1016/B978-0-12-384858-1.00007-2.Google Scholar
Zhang, G, et al. (2004) Negative regulation of prophenoloxidase (proPO) activation by a clip-domain serine proteinase homolog (SPH) from endoparasitoid venom. Insect Biochemistry and Molecular Biology 34, 477483. doi: 10.1016/j.ibmb.2004.02.009.Google Scholar
Zhu, J-Y, et al. (2009) Venom of Pteromalus puparum (Hymenoptera: Pteromalidae) induced endocrine changes in the hemolymph of its host, Pieris rapae (Lepidoptera: Pieridae). Archives of Insect Biochemistry and Physiology 71, 4553. doi: 10.1002/arch.20304.Google Scholar