[en] The parasitoid Leptopilina heterotoma has been used as a model system for more than 70 years, contributing greatly to diverse research areas in ecology and evolution. Here, we synthesized the large body of work on L. heterotoma with the aim to identify new research avenues that could be of interest also for researchers studying other parasitoids and insects. We start our review with a description of typical L. heterotomacharacteristics, as well as that of the higher taxonomic groups to which this species belongs. We then continue discussing host suitability and immunity, foraging behav-iors, as well as fat accumulation and life histories. We subsequently shift our focus towards parasitoid- parasitoid interactions, including L. heterotoma coexistence within the larger guild of Drosophila parasitoids, chemical communication, as well as mat-ing and population structuring. We conclude our review by highlighting the assets of L. heterotoma as a model system, including its intermediate life history syndromes, the ease of observing and collecting natural hosts and wasps, as well as recent genomic advances.
Disciplines :
Zoology Environmental sciences & ecology
Author, co-author :
Quicray, Maude ✱; Université de Liège - ULiège > TERRA Research Centre > Gestion durable des bio-agresseurs
Wilhelm, Léonore ✱; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs
Enriquez, Thomas ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs
He, Shulin; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs
Scheifler, Mathilde ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs
Visser, Bertanne ; Université de Liège - ULiège > TERRA Research Centre > Gestion durable des bio-agresseurs
✱ These authors have contributed equally to this work.
Language :
English
Title :
The Drosophila-parasitizing wasp Leptopilina heterotoma: A comprehensive model system in ecology and evolution
Fondation Fyssen [FR] FU - Universitaire Stichting [BE] F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
Funding number :
FNRS FC41573; FNRS J.0190.21; FNRS T.0186.20
Funding text :
Visser B, Enriquez E, He S, Scheifler M and Quicray M were funded by the Fonds National de Recherche Scientifique F.R.S.-FNRS (grants “J.0190.21”, “T.0186.20”, “FC 41573”). Enriquez T was further funded by the Fondation Fyssen. We would like to thank the University Foundation of Belgium for its contribution to publication fees.
Abram, P. K., Boivin, G., Moiroux, J., & Brodeur, J. (2017). Behavioural effects of temperature on ectothermic animals: Unifying thermal physiology and behavioural plasticity. Biological Reviews, 92(4), 1859–1876. https://doi.org/10.1111/brv.12312
Abram, P. K., Wang, X., Hueppelsheuser, T., Franklin, M. T., Daane, K. M., Lee, J. C., Lue, C.-H., Girod, P., Carrillo, J., Wong, W. H. L., Kula, R. R., Gates, M. W., Hogg, B. N., Moffat, C. E., Hoelmer, K. A., Sial, A. A., & Buffington, M. L. (2022). A coordinated sampling and identification methodology for larval parasitoids of spotted-wing Drosophila. Journal of Economic Entomology, 115, 922–942. https://doi.org/10.1093/jee/toab237
Addo-Bediako, A., Chown, S. L., & Gaston, K. J. (2000). Thermal tolerance, climatic variability and latitude. Proceedings of the Royal Society B, 267(1445), 739–745. https://doi.org/10.1098/rspb.2000.1065
Ahmed, M. Z., Breinholt, J. W., & Kawahara, A. Y. (2016). Evidence for common horizontal transmission of Wolbachia among butterflies and moths. BMC Evolutionary Biology, 16(1), 118. https://doi.org/10.1186/s12862-016-0660-x
Allemand, R., Fleury, F., Lemaitre, C., & Boulétreau, M. (1999). Dynamique des populations et interactions compétitives chez deux espèces de Leptopilina, parasitoïdes, dans la vallée du Rhône (Hymenoptera: Figitidae). Annales de la Société entomologique de France, 35, 97–103.
Amat, I., Castelo, M., Desouhant, E., & Bernstein, C. (2006). The influence of temperature and host availability on the host exploitation strategies of sexual and asexual parasitic wasps of the same species. Oecologia, 148(1), 153–161. https://doi.org/10.1007/s00442-005-0332-9
Anderl, I., Vesala, L., Ihalainen, T. O., Vanha-aho, L.-M., Andó, I., Rämet, M., & Hultmark, D. (2016). Transdifferentiation and proliferation in two distinct hemocyte lineages in Drosophila melanogaster larvae after wasp infection. PLoS Pathogens, 12(7), e1005746. https://doi.org/10.1371/journal.ppat.1005746
Ardeh, M. J., de Jong, P. W., & van Lenteren, J. C. (2005). Intra- and interspecific host discrimination in arrhenotokous and thelytokous Eretmocerus spp. Biological Control, 33(1), 74–80. https://doi.org/10.1016/j.biocontrol.2005.01.006
Arrese, E. L., & Soulages, J. L. (2010). Insect fat body: Energy, metabolism, and regulation. Annual Review of Entomology, 55, 207–225. https://doi.org/10.1146/annurev-ento-112408-085356
Ayasse, M., Paxton, R. J., & Tengö, J. (2001). Mating behaviour and chemical communication in the order hymenoptera. Annual Review of Entomology, 46, 31–78. https://doi.org/10.1146/annurev.ento.46.1.31
Bakker, K., Bagchee, S. N., Zwet, W. R., & Meelis, E. (1967). Host discrimination in Pseudocoila bochei (Hymenoptera: Cynipidae). Entomologia Experimentalis et Applicata, 10(3–4), 295–311. https://doi.org/10.1111/j.1570-7458.1967.tb02449.x
Bakker, K., Eijsackers, H. J. P., van Lenteren, J. C., & Meelis, E. (1972). Some models describing the distribution of eggs of the parasite Pseudeucoila bochei (Hym., Cynip.) over its hosts, larvae of Drosophila melanogaster. Oecologia, 10(1), 29–57. https://doi.org/10.1007/BF00822760
Bakker, K., Peulet, P., & Visser, M. E. (1990). The ability to distinguish between hosts containing different numbers of parasitoid eggs by the solitary parasitoid Leptopilina heterotoma (Thomson) (Hym., Cynip.). Netherlands Journal of Zoology, 40(3), 514–520. https://doi.org/10.1163/156854290X00064
Bakker, K., van Alphen, J. J. M., van Batenburg, F. H. D., van der Hoeven, N., Nell, H. W., van Strien-van Liempt, W. T. F. H., & Turlings, T. C. J. (1985). The function of host discrimination and superparasitization in parasitoids. Oecologia, 67, 572–576. https://doi.org/10.1007/BF00790029
Ballinger, M. J., & Perlman, S. J. (2017). Generality of toxins in defensive symbiosis: Ribosome-inactivating proteins and defense against parasitic wasps in Drosophila. PLoS Pathogens, 7(13), e1006431. https://doi.org/10.1371/journal.ppat.1006431
Bartelt, R. J., Schaner, A. M., & Jackson, L. L. (1985). Cis-vaccenyl acetate as an aggregation pheromone in Drosophila melanogaster. Journal of Chemical Ecology, 11, 1747–1756. https://doi.org/10.1007/BF01012124
Birsoy, K., Festuccia, W. T., & Laplante, M. (2013). A comparative perspective on lipid storage in animals. Journal of Cell Science, 126(7), 1541–1552. https://doi.org/10.1242/jcs.104992
Blacher, P., Huggins, T. J., & Bourke, A. F. G. (2017). Evolution of ageing, costs of reproduction and the fecundity-longevity trade-off in eusocial insects. Proceedings of the Royal Society B, 284, 20170380. https://doi.org/10.1098/rspb.2017.0380
Blaimer, B. B., Gotzek, D., Brady, S. G., & Buffington, M. L. (2020). Comprehensive phylogenomic analyses re-write the evolution of parasitism within cynipoid wasps. BMC Evolutionary Biology, 20(1), 155. https://doi.org/10.1186/s12862-020-01716-2
Blum, M. S. (1996). Semiochemical parsimony in the Arthropoda. Annual Review of Entomology, 41(1), 353–374. https://doi.org/10.1146/annurev.en.41.010196.002033
Bombin, A., & Reed, L. K. (2016). The changing biodiversity of Alabama Drosophila: Important impacts of seasonal variation, urbanization, and invasive species. Ecology and Evolution, 6(19), 7057–7069. https://doi.org/10.1002/ece3.2452
Bordenstein, S. R., Uy, J. J., & Werren, J. H. (2003). Host genotype determines cytoplasmic incompatibility type in the haplodiploid genus Nasonia. Genetics, 164, 223–233. https://doi.org/10.1093/genetics/164.1.223
Böttinger, L. C., Hofferberth, J., Ruther, J., & Stökl, J. (2019). Semiochemicals mediating defense, intraspecific competition, and mate finding in Leptopilina ryukyuensis and L. japonica (hymenoptera: Figitidae), parasitoids of Drosophila. Journal of Chemical Ecology, 45, 241–252. https://doi.org/10.1007/s10886-019-01052-w
Böttinger, L. C., Hüftlein, F., & Stökl, J. (2021). Mate attraction, chemical defense, and competition avoidance in the parasitoid wasp Leptopilina pacifica. Chemoecology, 31, 101–114. https://doi.org/10.1007/s00049-020-00331-3
Böttinger, L. C., & Stökl, J. (2020). Dispersal from natal patch correlates with the volatility of female sex pheromones in parasitoid wasps. Frontiers in Ecology and Evolution, 8, 557527. https://doi.org/10.3389/fevo.2020.557527
Boulton, R. A., Collins, L. A., & Shuker, D. M. (2015). Beyond sex allocation: The role of mating systems in sexual selection in parasitoid wasps: Sexual selection in parasitoid wasps. Biological Reviews, 90(2), 599–627. https://doi.org/10.1111/brv.12126
Boulton, R. A., Cook, N., Greenway, E. V., Glaser, G. L., Green, J., & Shuker, D. M. (2019). Local mate competition modifies the costs of mating in a mostly monandrous parasitoid wasp. Behavioral Ecology, 30, 417–425. https://doi.org/10.1093/beheco/ary181
Bozler, J., Kacsoh, B. Z., & Bosco, G. (2020). Maternal priming of offspring immune system in Drosophila. G3, 10(1), 165–175. https://doi.org/10.1534/g3.119.400852
Breeuwer, J. A. J., & Werren, J. H. (1990). Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. Nature, 346(6284), 558–560. https://doi.org/10.1038/346558a0
Buffington, M. L. (2007). The occurrence and phylogenetic implications of the ovipositor clip within the Figitidae (Insecta: Hymenoptera: Cynipoidea). Journal of Natural History, 41(33–36), 2267–2282. https://doi.org/10.1080/00222930701579732
Buffington, M. L., Giorgini, M., Lue, C.-H., Formisano, G., Cascone, P., Forshage, M., Driskell, A., & Guerrieri, E. (2020). Description of the aberrant Leptopilina lasallei n. sp., with an updated phylogeny of Leptopilina Förster (hymenoptera: Figitidae: Eucoilinae). Journal of Natural History, 54(9–12), 565–583. https://doi.org/10.1080/00222933.2020.1754483
Carton, Y., Bouletreau, M., van Alphen, J. J. M., & van Lenteren, J. C. (1986). The Drosophila parasitic wasps. In M. Ashburner, H. L. Carson, & J. N. Thompson (Eds.), The genetics and biology of Drosophila (Vol. 3, pp. 348–394). Academic Press.
Carton, Y., Frey, F., & Nappi, A. J. (2009). Parasite-induced changes in nitric oxide levels in Drosophila paramelanica. Journal of Parasitology, 95(5), 1134–1141. https://doi.org/10.1645/GE-2091.1
Carton, Y., Haouas, S., Marrakchi, M., & Hochberg, M. (1991). Two competing parasitoid species coexist in sympatry. Oikos, 60(2), 222–230. https://doi.org/10.2307/3544869
Chabert, S., Allemand, R., Poyet, M., Eslin, P., & Gibert, P. (2012). Ability of European parasitoids (hymenoptera) to control a new invasive Asiatic pest, Drosophila suzukii. Biological Control, 63(1), 40–47. https://doi.org/10.1016/j.biocontrol.2012.05.005
Chabora, P. C., Smolin, S. J., & Kopelman, A. H. (1979). The life history of Pseudeucoila sp., a protelian parasite of Drosophila. Annals of the Entomological Society of America, 72(4), 495–499. https://doi.org/10.1093/aesa/72.4.495
Chang, H., Guo, X., Guo, S., Yang, N., & Huang, Y. (2021). Trade-off between flight capability and reproduction in Acridoidea (Insecta: Orthoptera). Ecology and Evolution, 11(23), 16849–16861. https://doi.org/10.1002/ece3.8317
Charnov, E. L. (1976). Optimal foraging, the marginal value theorem. Theoretical Population Biology, 9(2), 129–136. https://doi.org/10.1016/0040-5809(76)90040-X
Charnov, E. L. (1979). The genetical evolution of patterns of sexuality: Darwinian fitness. The American Naturalist, 113(4), 465–480. https://doi.org/10.1086/283407
Charnov, E. L. (1982). The theory of sex allocation. (MPB-18), 18. Princeton University Press. https://doi.org/10.2307/j.ctvx8b6km
Charnov, E. L., Los-den Hartogh, R., Jones, W. J., & van den Assem, J. (1981). Sex ratio evolution in a variable environment. Nature, 289, 27–33. https://doi.org/10.1038/289027a0
Chiu, H., & Govind, S. (2002). Natural infection of D. melanogaster by virulent parasitic wasps induces apoptotic depletion of hematopoietic precursors. Cell Death and Differentiation, 9, 1379–1381. https://doi.org/10.1038/sj.cdd.4401134
Chiu, H., Morales, J., & Govind, S. (2006). Identification and immuno-electron microscopy localization of p40, a protein component of immunosuppressive virus-like particles from Leptopilina heterotoma, a virulent parasitoid wasp of Drosophila. Journal of General Virology, 87(2), 461–470. https://doi.org/10.1099/vir.0.81474-0
Clark, A. B. (1978). Sex ratio and local resource competition in a prosimian primate. Science, 201(4351), 163–165. https://doi.org/10.1126/science.201.4351.163
Colinet, D., Deleury, E., Anselme, C., Cazes, D., Poulain, J., Azema-Dossat, C., Belghazi, M., Gatti, J.-L., & Poirié, M. (2013). Extensive inter- and intraspecific venom variation in closely related parasites targeting the same host: The case of Leptopilina parasitoids of Drosophila. Insect Biochemistry and Molecular Biology, 43(7), 601–611. https://doi.org/10.1016/j.ibmb.2013.03.010
Colinet, D., Kremmer, L., Lemauf, S., Rebuf, C., Gatti, J.-L., & Poirié, M. (2014). Development of RNAi in a Drosophila endoparasitoid wasp and demonstration of its efficiency in impairing venom protein production. Journal of Insect Physiology, 63, 56–61. https://doi.org/10.1016/j.jinsphys.2014.02.011
Cook, J. M. (1993). Sex determination in the hymenoptera: A review of models and evidence. Heredity, 71, 421–435. https://doi.org/10.1038/hdy.1993.157
Corbin, C., Jones, J. E., Chrostek, E., Fenton, A., & Hurst, G. D. D. (2021). Thermal sensitivity of the Spiroplasma – Drosophila hydei protective symbiosis: The best of climes, the worst of climes. Molecular Ecology, 30(5), 1336–1344. https://doi.org/10.1111/mec.15799
Coulette, Q., Lemauf, S., Colinet, D., Prévost, G., Anselme, C., Poirié, M., & Gatti, J.-L. (2017). Biochemical characterization and comparison of aspartylglucosaminidases secreted in venom of the parasitoid wasps Asobara tabida and Leptopilina heterotoma. PLoS One, 12(7), e0181940. https://doi.org/10.1371/journal.pone.0181940
Daane, K. M., Wang, X.-G., Biondi, A., Miller, B., Miller, J. C., Riedl, H., Shearer, P. W., Guerrieri, E., Giorgini, M., Buffington, M., van Achterberg, K., Song, Y., Kang, T., Yi, H., Jung, C., Lee, D. W., Chung, B.-K., Hoelmer, K. A., & Walton, V. M. (2016). First exploration of parasitoids of Drosophila suzukii in South Korea as potential classical biological agents. Journal of Pest Science, 89, 823–835. https://doi.org/10.1007/s10340-016-0740-0
Dalla Benetta, E., Chaverra-Rodriguez, D., Rasgon, J. L., & Akbari, O. S. (2020). Pupal and adult injections for RNAi and CRISPR gene editing in Nasonia vitripennis. Journal of Visualized Experiements, 166, e61892. https://doi.org/10.3791/61892
Damiens, D., & Boivin, G. (2005). Male reproductive strategy in Trichogramma evanescens: Sperm production and allocation to females. Physiological Entomology, 30, 241–247. https://doi.org/10.1111/j.1365-3032.2005.00453.x
de Bruijn, J. A. C., Vosteen, I., Vet, L. E. M., Smid, H. M., & de Boer, J. G. (2021). Multi-camera field monitoring reveals costs of learning for parasitoid foraging behaviour. Journal of Animal Ecology, 90(7), 1635–1646. https://doi.org/10.1111/1365-2656.13479
Delava, E., Fleury, F., & Gibert, P. (2022). Differentiation of thermal reaction norms between marginal and core populations of a northward expanding parasitoid. BioRxiv. https://doi.org/10.1101/2022.04.26.489532
Delpuech, J.-M., & Allemand, R. (2011). Side effects of fungicides on the abundance and the species diversity of the natural populations of Drosophila and their hymenopterous parasitoids in orchards. Phytoparasitica, 39, 429–435. https://doi.org/10.1007/s12600-011-0180-6
Di Giovanni, D., Lepetit, D., Guinet, B., Bennetot, B., Boulesteix, M., Couté, Y., Bouchez, O., Ravallec, M., & Varaldi, J. (2020). A behavior-manipulating virus relative as a source of adaptive genes for Drosophila parasitoids. Molecular Biology and Evolution, 37, 2791–2807. https://doi.org/10.1093/molbev/msaa030
Dicke, M., van Lenteren, J. C., Boskamp, G. J. F., & van Dongen-van Leeuwen, E. (1984). Chemical stimuli in host-habitat location by Leptopilina heterotoma (Thomson) (hymenoptera: Eucoilidae), a parasite of Drosophila. Journal of Chemical Ecology, 37(10), 695–712. https://doi.org/10.1007/BF00988537
Dicke, M., van Lenteren, J. C., Boskamp, G. J. F., & Van Voorst, R. (1985). Intensification and prolongation of host searching in Leptopilina heterotoma (Thomson) (hymenoptera: Eucoilidae) through a kairomone produced by Drosophila melanogaster. Journal of Chemical Ecology, 11, 125–135. https://doi.org/10.1007/bf00987611
Driessen, G., van Alphen, J. J. M., & Hemerik, L. (1990). Drosophila species, breeding in the stinkhorn (Phallus impudicus Pers.) and their larval parasitoids. Netherlands Journal of Zoology, 40(3), 409–427. https://doi.org/10.1163/156854290X00019
Eijs, I. E. M., Ellers, J., & van Duinen, G.-J. (1998). Feeding strategies in drosophilid parasitoids: The impact of natural food resources on energy reserves in females. Ecological Entomology, 23(2), 133–138. https://doi.org/10.1046/j.1365-2311.1998.00117.x
Eijsackers, H. J. P., & Bakker, K. (1971). Elimination by physical attack of supernumerary larvae of Pseudeucoila bochei Weld (Cynipidae) in their hosts, larvae of Drosophila. Netherlands Journal of Zoology, 21(2), 205–207. https://doi.org/10.1163/002829671X00168
Ellers, J. (1996). Fat and eggs: An alternative method to measure the trade-off between survival and reproduction in insect parasitoids. Netherlands Journal of Zoology, 46(3–4), 227–235. https://doi.org/10.1163/156854295X00186
Ellers, J., & Jervis, M. A. (2004). Why are so few parasitoid wasp species pro-ovigenic? Evolutionary Ecology, 6(7), 993–1002.
Ellers, J., van Alphen, J. J. M., & Sevenster, J. G. (1998). A field study of size-fitness relationship in the parasitoid Asobara tabida. Journal of Animal Ecology, 67(2), 318–324. http://www.jstor.org/stable/2647500
El-Sayed, A. (2022). The Pherobase: Database of pheromones and semiochemicals. http://www.pherobase.com
Enriquez, T., Lievens, V., Nieberding, C. M., & Visser, B. (2022). Pupal size as a proxy for fat content in laboratory-reared and field-collected Drosophila species. Scientific Reports, 12, 12855. https://doi.org/10.1038/s41598-022-15325-0
Fagerström, T., & Wiklund, C. (1982). Why do males emerge before females? Protandry as a mating strategy in male and female butterflies. Oecologia, 52(2), 164–166. https://doi.org/10.1007/bf00363830
Fauvergue, X., Fleury, F., Lemaitre, C., & Allemand, R. (1999). Parasitoid mating structures when hosts are patchily distributed: Field and laboratory experiments with Leptopilina boulardi and L. heterotoma. Oikos, 86(2), 344–356. https://doi.org/10.2307/3546451
Fauvergue, X., Lo Genco, A., & Lo Pinto, M. (2008). Virgins in the wild: Mating status affects the behavior of a parasitoid foraging in the field. Oecologia, 156(4), 913–920. https://doi.org/10.1007/s00442-008-1037-7
Ferrarese, R., Morales, J., Fimiarz, D., Webb, B. A., & Govind, S. (2009). A supracellular system of actin-lined canals controls biogenesis and release of virulence factors in parasitoid venom glands. Journal of Experimental Biology, 212(14), 2261–2268. https://doi.org/10.1242/jeb.025718
Fisher, R. A. (1930). The genetical theory of natural selection. Clarendon. https://doi.org/10.5962/bhl.title.27468
Fleury, F., Allemand, R., Vavre, F., Fouillet, P., & Boulétreu, M. (2000). Adaptive significance of a circadian clock: Temporal segregation of activities reduces intrinsic competitive inferiority in Drosophila parasitoids. Proceedings: Biological Sciences, 267(1447), 1005–1010.
Fleury, F., Gibert, P., Ris, N., & Allemand, R. (2009). Chapter 1: Ecology and life history evolution of frugivorous Drosophila parasitoids. Advances in Parasitology, 70, 3–44. https://doi.org/10.1016/S0065-308X(09)70001-6
Fleury, F., Ris, N., Allemand, R., Fouillet, P., Carton, Y., & Bouletreau, M. (2004). Ecological and genetic interactions in Drosophila-parasitoids communities: A case study with D. melanogaster, D. simulans and their common Leptopilina parasitoids in South-Eastern France. Genetica, 120(1–3), 181–194. https://doi.org/10.1023/b:gene.0000017640.78087.9e
Fleury, F., Vavre, F., Ris, N., Fouillet, P., & Boulétreau, M. (2000). Physiological cost induced by the maternally-transmitted endosymbiont Wolbachia in the Drosophila parasitoid Leptopilina heterotoma. Parasitology, 121(5), 493–500. https://doi.org/10.1017/S0031182099006599
Fontal-Cazalla, F. M., Buffington, M. L., Nordlander, G., Liljeblad, J., Ros-Farre, P., Nieves-Aldrey, J. L., Pujade-Villar, J., & Ronquist, F. (2002). Phylogeny of the Eucoilinae (hymenoptera: Cynipoidea: Figitidae). Cladistics, 18(2), 154–199. https://doi.org/10.1111/j.1096-0031.2002.tb00147.x
Forbes, A. A., Bagley, R. K., Beer, M. A., Hippee, A. C., & Widmayer, H. A. (2018). Quantifying the unquantifiable: Why hymenoptera, not Coleoptera, is the most speciose animal order. BMC Ecology, 18(21), 1–11. https://doi.org/10.1186/s12898-018-0176-x
Frost, C. L., Pollock, S. W., Smith, J. E., & Hughes, W. O. H. (2014). Wolbachia in the flesh: Symbiont intensities in germ-line and somatic tissues challenge the conventional view of Wolbachia transmission routes. PLoS One, 9(7), e95122. https://doi.org/10.1371/journal.pone.0095122
Fytrou, A., Schofield, P. G., Kraaijeveld, A. R., & Hubbard, S. F. (2006). Wolbachia infection suppresses both host defence and parasitoid counter-defence. Proceedings of the Royal Society B, 273(1588), 791–796. https://doi.org/10.1098/rspb.2005.3383
Germain, R. M., Williams, J. L., Schluter, D., & Angert, A. L. (2018). Moving character displacement beyond characters using contemporary coexistence theory. Trends in Ecology and Evolution, 33(2), 74–84. https://doi.org/10.1016/j.tree.2017.11.002
Gibson, G. A. P. (2009). Revision of new world Spalangiinae (hymenoptera: Pteromalidae). Zootaxa, 2259(1), 1–159. https://doi.org/10.11646/zootaxa.2259.1.1
Giorgini, M., Wang, X.-G., Wang, Y., Chen, F.-S., Hougardy, E., Zhang, H.-M., Chen, Z.-Q., Chen, H.-Y., Liu, C.-X., Cascone, P., Formisano, G., Carvalho, G. A., Biondi, A., Buffington, M., Daane, K. M., Hoelmer, K. A., & Guerrieri, E. (2019). Exploration for native parasitoids of Drosophila suzukii in China reveals a diversity of parasitoid species and narrow host range of the dominant parasitoid. Journal of Pest Science, 92, 509–522. https://doi.org/10.1007/s10340-018-01068-3
Giraldeau, L.-A., & Boivin, G. (2008). Risk assessment and host exploitation strategies in insect parasitoids. In E. Wajnberg, C. Bernstein, & J. J. M. van Alphen (Eds.), Behavioral ecology of insect parasitoids: From theoretical approaches to field applications (pp. 212–227). Blackwell Publishing. https://doi.org/10.1002/9780470696200.ch10
Girod, P., Borowiec, N., Buffington, M., Chen, G., Fang, Y., Kimura, M. T., Peris-Felipo, F. J., Ris, N., Wu, H., Xiao, C., Zhang, J., Aebi, A., Haye, T., & Kenis, M. (2018). The parasitoid complex of D. suzukii and other fruit feeding Drosophila species in Asia. Scientific Reports, 8(1), 11839. https://doi.org/10.1038/s41598-018-29555-8
Girod, P., Rossignaud, L., Haye, T., Turlings, T. C. J., & Kenis, M. (2018). Development of Asian parasitoids in larvae of Drosophila suzukii feeding on blueberry and artificial diet. Journal of Applied Entomology, 142(5), 483–494. https://doi.org/10.1111/jen.12496
Godfray, H. C. J. (1988). Virginity in haplodiploid populations: A study on fig wasps. Ecological Entomology, 13(3), 283–291.
Godfray, H. C. J. (1990). The causes and consequences of constrained sex allocation in haplodiploid animals. Journal of Evolutionary Biology, 3(1–2), 3–17. https://doi.org/10.1046/j.1420-9101.1990.3010003.x
Godfray, H. C. J. (1994). Parasitoids: Behavioral and evolutionary ecology. In J. R. Krebs & T. Clutton-Brock (Eds.), Monographs in behavior and ecology (Vol. 67). Princeton University Press. https://doi.org/10.2307/j.ctvs32rmp
Godfray, H. C. J., & Cook, J. M. (1997). Mating systems of parasitoid wasps. In J. C. Choe & B. J. Crespi (Eds.), The evolution of mating systems in insects and arachnids (pp. 211–225). Cambridge University Press. https://doi.org/10.1017/CBO9780511721946.013
Godfray, H. C. J., & Grafen, A. (1988). Unmatedness and the evolution of eusociality. The American Naturalist, 131(2), 303–305.
Godfray, H. C. J., & Hardy, I. C. W. (1990). Estimating the frequency of constrained sex allocation in field populations of hymenoptera. Behaviour, 114(1), 137–147. https://doi.org/10.1163/156853990X00086
Goecks, J., Mortimer, N. T., Mobley, J. A., Bowersock, G. J., Taylor, J., & Schlenke, T. A. (2013). Integrative approach reveals composition of endoparasitoid wasp venoms. PLoS One, 8(5), e64125. https://doi.org/10.1371/journal.pone.0064125
Gokhman, V. E. (2018). Dimensions and borderlines of parasitoid hymenoptera species: A paradigm shift? Biology Bulletin Reviews, 8(3), 227–233. https://doi.org/10.1134/S2079086418030052
Gompel, N., & Carroll, S. B. (2003). Genetic mechanisms and constraints governing the evolution of correlated traits in drosophilid flies. Nature, 424(6951), 931–935. https://doi.org/10.1038/nature01787
Grasswitz, T. R., & Jones, G. R. (2002). Chemical ecology. Encyclopedia of Life Sciences. https://doi.org/10.1038/npg.els.0003265
Haccou, P., Vlas, S. J. D., Alphen, J. J. M. V., & Visser, M. E. (1991). Information processing by foragers: Effects of intra-patch experience on the leaving tendency of Leptopilina heterotoma. The Journal of Animal Ecology, 60(1), 93–106. https://doi.org/10.2307/5447
Hahn, D. A., & Denlinger, D. L. (2011). Energetics of insect diapause. Annual Review of Entomology, 56(1), 103–121. https://doi.org/10.1146/annurev-ento-112408-085436
Hamilton, W. D. (1967). Extraordinary sex ratios: A sex-ratio theory for sex linkage and inbreeding has new implications in cytogenetics and entomology. Science, 156(3774), 477–488. https://doi.org/10.1126/science.156.3774.477
Hardy, I. C. W. (1994). Sex ratio and mating structure in the parasitoid hymenoptera. Oikos, 69(1), 3–20. https://doi.org/10.2307/3545278
Harvey, J. A., Snaas, H., Malcicka, M., Visser, B., & Bezemer, T. M. (2014). Small-scale spatial resource partitioning in a hyperparasitoid community. Arthropod-Plant Interactions, 8(5), 393–401. https://doi.org/10.1007/s11829-014-9319-y
Harvey, J. A., & Strand, M. R. (2002). The developmental strategies of endoparasitoid wasps vary with host feeding ecology. Ecology, 83(9), 2439–2451. https://doi.org/10.1890/0012-9658(2002)083[2439:tdsoew]2.0.co;2
Heavner, M. E., Gueguen, G., Rajwani, R., Pagan, P. E., Small, C., & Govind, S. (2013). Partial venom gland transcriptome of a Drosophila parasitoid wasp, Leptopilina heterotoma, reveals novel and shared bioactive profiles with stinging hymenoptera. Gene, 526(2), 195–204. https://doi.org/10.1016/j.gene.2013.04.080
Hedlund, K., Vet, L. E. M., & Dicke, M. (1996). Generalist and specialist parasitoid strategies of using odours of adult drosophilid flies when searching for larval hosts. Oikos, 77(3), 390–398. https://doi.org/10.2307/3545929
Heimpel, G. E., & de Boer, J. G. (2008). Sex determination in the hymenoptera. Annual Review of Entomology, 53(1), 209–230. https://doi.org/10.1146/annurev.ento.53.103106.093441
Hemerik, L., Van Der Hoeven, N., & van Alphen, J. J. M. (2002). Egg distributions and the information a solitary parasitoid has and uses for its oviposition decisions. Acta Biotheoretica, 50(3), 167–188. https://doi.org/10.1023/a:1016543310896
Henneman, M. L., Papaj, D. R., Figueredo, A. J., & Vet, L. E. M. (1995). Egg-laying experience and acceptance of parasitized hosts by the parasitoid, Leptopilina heterotoma (hymenoptera: Eucoilidae). Journal of Insect Behavior, 8(3), 331–342. https://doi.org/10.1007/BF01989362
Herren, J. K., Paredes, J. C., Schüpfer, F., Arafah, K., Bulet, P., & Lemaitre, B. (2014). Insect endosymbiont proliferation is limited by lipid availability. eLife, 3, e02964. https://doi.org/10.7554/eLife.02964
Higareda Alvear, V. M., Mateos, M., Cortez, D., Tamborindeguy, C., & Martinez-Romero, E. (2021). Differential gene expression in a tripartite interaction: Drosophila, Spiroplasma and parasitic wasps. PeerJ, 9, e11020. https://doi.org/10.7717/peerj.11020
Howe, R. W. (1967). Temperature effects on embryonic development in insects. Annual Review of Entomology, 12(1), 15–42. https://doi.org/10.1146/annurev.en.12.010167.000311
Huang, J., Chen, J., Fang, G., Pang, L., Zhou, S., Zhou, Y., Pan, Z., Zhang, Q., Sheng, Y., Lu, Y., Liu, Z., Zhang, Y., Li, G., Shi, M., Chen, X., & Zhan, S. (2021). Two novel venom proteins underlie divergent parasitic strategies between a generalist and a specialist parasite. Nature Communications, 12, 234. https://doi.org/10.1038/s41467-020-20332-8
Hubbard, S. F., & Cook, R. M. (1978). Optimal foraging by parasitoid wasps. The Journal of Animal Ecology, 47, 593–604. https://doi.org/10.2307/3803
Ideo, S., Watada, M., Mitsui, H., & Kimura, M. T. (2008). Host range of Asobara japonica (hymenoptera: Braconidae), a larval parasitoid of drosophilid flies. Entomological sciences, 11(1), 1–6. https://doi.org/10.1111/j.1479-8298.2007.00244.x
Isidoro, N., Bin, F., & Romani, R. (1999). Diversity and function of male antennal glands in Cynipoidea (hymenoptera). Zoologica Scripta, 28(1–2), 165–174. https://doi.org/10.1046/j.1463-6409.1999.00013.x
Jacob, S., & Boivin, G. (2005). Costs and benefits of polyandry in the egg parasitoid Trichogramma evanescens Westwood (hymenoptera: Trichogrammatidae). Biological Control, 32(2), 311–318. https://doi.org/10.1016/j.biocontrol.2004.10.009
Janssen, A. (1989). Optimal host selection by Drosophila parasitoids in the field. Functional Ecology, 3(4), 469–479. https://doi.org/10.2307/2389621
Janssen, A., Driessen, G., Haan, M. D., & Roodbol, N. (1988). The impact of parasitoids on natural populations on temperate woodland Drosophila. Netherlands Journal of Zoology, 38(1), 61–73. https://doi.org/10.1163/156854288x00049
Janssen, A., van Alphen, J. J. M., Sabelis, M. W., & Bakker, K. (1995). Specificity of odour-mediated avoidance of competition in Drosophila parasitoids. Behavioral Ecology and Sociobiology, 36, 229–235. https://doi.org/10.1007/BF00165831
Jeffs, C. T., Terry, J. C. D., Higgie, M., Jandová, A., Konvičková, H., Brown, J. J., Lue, C. H., Schiffer, M., O'Brien, E. K., Bridle, J., Hrček, J., & Lewis, O. T. (2021). Molecular analyses reveal consistent food web structure with elevation in rainforest Drosophila – Parasitoid communities. Ecography, 44(3), 403–413. https://doi.org/10.1111/ecog.05390
Jenni, W. (1951). Beitrag zur morphologie und biologie der cynipide Pseudeucoila bochei weld, eines larvenparasiten von Drosophila melanogaster meig. Acta Zoologica, 32(3), 177–254. https://doi.org/10.1111/j.1463-6395.1951.tb00468.x
Kacsoh, B. Z., & Schlenke, T. A. (2012). High hemocyte load is associated with increased resistance against parasitoids in Drosophila suzukii, a relative of D. melanogaster. PLoS ONE, 7(4), e34721. https://doi.org/10.1371/journal.pone.0034721
Keebaugh, E. S., & Schlenke, T. A. (2012). Adaptive evolution of a novel Drosophila lectin induced by parasitic wasp attack. Molecular Biology and Evolution, 29(2), 565–577. https://doi.org/10.1093/molbev/msr191
Kenis, M., Tonina, L., Eschen, R., van der Sluis, B., Sancassani, M., Mori, N., Haye, T., & Helsen, H. (2016). Non-crop plants used as hosts by Drosophila suzukii in Europe. Journal of Pest Science, 89, 735–748. https://doi.org/10.1007/s10340-016-0755-6
Kimura, M. T. (2019). Overwintering of reproductively mature females of a pro-ovigenic parasitic wasp, Leptopilina heterotoma (hymenoptera: Figitidae). Entomological Science, 22(3), 264–269. https://doi.org/10.1111/ens.12365
Kimura, M. T., & Mitsui, H. (2020). Drosophila parasitoids (hymenoptera) of Japan. Entomological Science, 23(4), 359–368. https://doi.org/10.1111/ens.12432
Kimura, M. T., Ohtsu, T., Yoshida, T., Awasaki, T., & Lin, F.-J. (1994). Climatic adaptations and distributions in the Drosophila takahashii species subgroup (Diptera: Drosophilidae). Journal of Natural History, 28(2), 401–409. https://doi.org/10.1080/00222939400770181
King, A. J., & Marshall, H. H. (2022). Optimal foraging. Current Biology, 32(12), R680–R683. https://doi.org/10.1016/j.cub.2022.04.072
King, B. (1987). Offspring sex ratios in parasitoid wasps. Quarterly Review of Biology, 62(4), 367–396. https://doi.org/10.1086/415618
King, B. (1993). Sex ratio manipulation by parasitoid wasps. In D. L. Wrensch & M. A. Ebbert (Eds.), Evolution and diversity of sex ratio in insects and mites (pp. 418–441). Chapman & Hall.
Klepsatel, P., Knoblochová, D., Girish, T. N., Dircksen, H., & Gáliková, M. (2020). The influence of developmental diet on reproduction and metabolism in Drosophila. BMC Evolutionary Biology, 20(1), 93. https://doi.org/10.1186/s12862-020-01663-y
Klepsatel, P., Procházka, E., & Gáliková, M. (2018). Crowding of Drosophila larvae affects lifespan and other life-history traits via reduced availability of dietary yeast. Experimental Gerontology, 110, 298–308. https://doi.org/10.1016/j.exger.2018.06.016
Knoll, V., Ellenbroek, T., Romeis, J., & Collatz, J. (2017). Seasonal and regional presence of hymenopteran parasitoids of Drosophila in Switzerland and their ability to parasitize the invasive Drosophila suzukii. Scientific Reports, 7, 40697. https://doi.org/10.1038/srep40697
Kohl, J., Huoviala, P., & Jefferis, G. S. (2015). Pheromone processing in Drosophila. Current Opinion in Neurobiology, 34, 149–157. https://doi.org/10.1016/j.conb.2015.06.009
Kopelman, A. H., & Chabora, P. C. (1984). Immature stages of Leptopilina boulardi (hymenoptera: Eucoilidae), a rotelean arasite of Drosophila spp. (Diptera: Drosophilidae). Annals of the Entomological Society of America, 77(3), 264–269. https://doi.org/10.1093/aesa/77.3.264
Kraaijeveld, A. R., & Godfray, H. C. J. (1999). Geographic patterns in the evolution of resistance and virulence in Drosophila and its parasitoids. The American Naturalist, 153(S5), S61–S74. https://doi.org/10.1086/303212
Kraaijeveld, A. R., & Godfray, H. C. J. (2009). Chapter 10: Evolution of host resistance and parasitoid counter-resistance. In G. Prevost (Ed.) Advances in parasitology (Vol. 70, pp. 257–280). Elsevier. https://doi.org/10.1016/S0065-308X(09)70010-7
Krams, I. A., Krams, R., Jõers, P., Munkevics, M., Trakimas, G., Luoto, S., Eichler, S., Butler, D. M., Merivee, E., Must, A., Rantala, M. J., Contreras-Garduño, J., & Krama, T. (2020). Developmental speed affects ecological stoichiometry and adult fat reserves in Drosophila melanogaster. Animal Biology, 71(1), 1–20. https://doi.org/10.1163/15707563-bja10043
Kremmer, L., Thaon, M., Borowiec, N., David, J., Poirié, M., Gatti, J.-L., & Ris, N. (2017). Field monitoring of Drosophila suzukii and associated communities in south eastern France as a pre-requisite for classical biological control. Insects, 8(4), 124. https://doi.org/10.3390/insects8040124
Kronfeld-Schor, N., & Dayan, T. (2003). Partitioning of time as an ecological resource. Annual Review of Ecology, Evolution and Systematics, 34(1), 153–181. https://doi.org/10.1146/annurev.ecolsys.34.011802.132435
Kuntz, S. G., & Eisen, M. B. (2014). Drosophila embryogenesis scales uniformly across temperature in developmentally diverse species. PLoS Genetics, 10(4), e1004293. https://doi.org/10.1371/journal.pgen.1004293
Lacovone, A., Ris, N., Poirié, M., & Gatti, J.-L. (2018). Time-course analysis of Drosophila suzukii interaction with endoparasitoid wasps evidences a delayed encapsulation response compared to D. melanogaster. PLoS ONE, 13(8), e0201573. https://doi.org/10.1371/journal.pone.0201573
Le Lann, C., Lodi, M., & Ellers, J. (2014). Thermal change alters the outcome of behavioural interactions between antagonistic partners. Ecological Entomology, 39(5), 578–588. https://doi.org/10.1111/een.12135
Lease, H. M., & Wolf, B. O. (2011). Lipid content of terrestrial arthropods in relation to body size, phylogeny, ontogeny and sex. Physiological Entomology, 36(1), 29–38. https://doi.org/10.1111/j.1365-3032.2010.00767.x
Lee, J. C., Dreves, A. J., Cave, A. M., Kawai, S., Isaacs, R., Miller, J. C., Van Timmeren, S., & Bruck, D. J. (2015). Infestation of wild and ornamental noncrop fruits by Drosophila suzukii (Diptera: Drosophilidae). Annals of the Entomological Society of America, 108(2), 117–129. https://doi.org/10.1093/aesa/sau014
Li, K.-M., Au, L. Y. C., Douglah, D., Chong, A., White, B. J., Ferree, P. M., & Akbari, O. S. (2017). Generation of heritable germline mutations in the jewel wasp Nasonia vitripennis using CRISPR/Cas9. Scientific Reports, 7(1), 901. https://doi.org/10.1038/s41598-017-00990-3
Li, K.-M., Ren, L.-Y., Zhang, Y.-J., Wu, K.-M., & Guo, Y.-Y. (2012). Knockdown of microplitis mediator odorant receptor involved in the sensitive detection of two chemicals. Journal of Chemical Ecology, 38(3), 287–294. https://doi.org/10.1007/s10886-012-0085-y
Lof, M. E., De Gee, M., Dicke, M., Gort, G., & Hemerik, L. (2013). Exploitation of chemical signaling by parasitoids: Impact on host population dynamics. Journal of Chemical Ecology, 39(6), 752–763. https://doi.org/10.1007/s10886-013-0298-8
Losos, J. B. (2000). Ecological character displacement and the study of adaptation. Proceedings of the National Academy of Sciences of the United States of America, 97(11), 5693–5695. https://doi.org/10.1073/pnas.97.11.5693
Lue, C.-H., Borowy, D., Buffington, M. L., & Leips, J. (2018). Geographic and seasonal variation in species diversity and community composition of frugivorous Drosophila (Diptera: Drosophilidae) and their Leptopilina (hymenoptera: Figitidae) parasitoids. Environmental Entomology, 47(5), 1096–1106. https://doi.org/10.1093/ee/nvy114
Lue, C.-H., Buffington, M. L., Scheffer, S., Lewis, M., Elliott, T. A., Lindsey, A. R. I., Driskell, A., Jandova, A., Kimura, M. T., Carton, Y., Kula, R. R., Schlenke, T. A., Mateos, M., Govind, S., Varaldi, J., Guerrieri, E., Giorgini, M., Wang, X., Hoelmer, K., … Hrcek, J. (2021). DROP: Molecular voucher database for identification of Drosophila parasitoids. Molecular Ecology Resources, 21(7), 2437–2454. https://doi.org/10.1111/1755-0998.13435
Lue, C.-H., Driskell, A. C., Leips, J., & Buffington, M. L. (2016). Review of the genus Leptopilina (hymenoptera, Cynipoidea, Figitidae, Eucoilinae) from the eastern United States, including three newly described species. Journal of Hymenoptera Research, 53, 35–76. https://doi.org/10.3897/jhr.53.10369
Lynch, J. (2006). A method for parental RNA interference in the wasp Nasonia vitripennis. Nature Protocols, 1(1), 486–494. https://doi.org/10.1038/nprot.2006.70
Lynch, Z. R., Schlenke, T. A., Morran, L. T., & de Roode, J. C. (2017). Ethanol confers differential protection against generalist and specialist parasitoids of Drosophila melanogaster. PLoS ONE, 12(7), e0180182. https://doi.org/10.1371/journal.pone.0180182
Lynch, Z. R., Schlenke, T. A., & Roode, J. C. (2016). Evolution of behavioural and cellular defences against parasitoid wasps in the Drosophila melanogaster subgroup. Journal of Evolutionary Biology, 29(5), 1016–1029. https://doi.org/10.1111/jeb.12842
Mackay, T. F. C., Richards, S., Stone, E. A., Barbadilla, A., Ayroles, J. F., Zhu, D., Casillas, S., Han, Y., Magwire, M. M., Cridland, J. M., Richardson, M. F., Anholt, R. R. H., Barrón, M., Bess, C., Blankenburg, K. P., Carbone, M. A., Castellano, D., Chaboub, L., Duncan, L., … Gibbs, R. A. (2012). The Drosophila melanogaster genetic reference panel. Nature, 482(7384), 173–178. https://doi.org/10.1038/nature10811
Markow, T. A., & O'Grady, P. M. (2005). Evolutionary genetics of reproductive behavior in Drosophila: Connecting the dots. Annual Review of Genetics, 39(1), 263–291. https://doi.org/10.1146/annurev.genet.39.073003.112454
Markow, T. A., & O'Grady, P. M. (2008). Reproductive ecology of Drosophila. Functional Ecology, 22(5), 747–759. https://doi.org/10.1111/j.1365-2435.2008.01457.x
Markus, R., Laurinyecz, B., Kurucz, E., Honti, V., Bajusz, I., Sipos, B., Somogyi, K., Kronhamn, J., Hultmark, D., & Ando, I. (2009). Sessile hemocytes as a hematopoietic compartment in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America, 106(12), 4805–4809. https://doi.org/10.1073/pnas.0801766106
Mazzetto, F., Marchetti, E., Amiresmaeili, N., Sacco, D., Francati, S., Jucker, C., Dindo, M. L., Lupi, D., & Tavella, L. (2016). Drosophila parasitoids in northern Italy and their potential to attack the exotic pest Drosophila suzukii. Journal of Pest Science, 89(3), 837–850. https://doi.org/10.1007/s10340-016-0746-7
Meiners, T. (2003). Associative learning of complex odours in parasitoid host location. Chemical Senses, 28(3), 231–236. https://doi.org/10.1093/chemse/28.3.231
Mery, F., & Kawecki, T. J. (2005). A cost of long-term memory in Drosophila. Science, 308(5725), 1148. https://doi.org/10.1126/science.1111331
Milan, N. F., Kacsoh, B. Z., & Schlenke, T. A. (2012). Alcohol consumption as self-medication against blood-borne parasites in the fruit fly. Current Biology, 22(6), 488–493. https://doi.org/10.1016/j.cub.2012.01.045
Mitsui, H., & Kimura, M. T. (2010). Distribution, abundance and host association of two parasitoid species attacking frugivorous drosophilid larvae in Central Japan. European Journal of Entomology, 107(4), 535–540. https://doi.org/10.14411/eje.2010.061
Mitsui, H., Van Achterberg, K., Nordlander, G., & Kimura, M. T. (2007). Geographical distributions and host associations of larval parasitoids of frugivorous Drosophilidae in Japan. Journal of Natural History, 41(25–28), 1731–1738. https://doi.org/10.1080/00222930701504797
Moiroux, J., Boivin, G., & Brodeur, J. (2015). Temperature influences host instar selection in an aphid parasitoid: Support for the relative fitness rule. Biological Journal of the Linnean Society, 115(4), 792–801. https://doi.org/10.1111/bij.12545
Moiroux, J., Le Lann, C., Seyahooei, M. A., Vernon, P., Pierre, J.-S., van Baaren, J., & van Alphen, J. J. M. (2010). Local adaptations of life-history traits of a Drosophila parasitoid, Leptopilina boulardi: Does climate drive evolution? Ecological Entomology, 35(6), 727–736. https://doi.org/10.1111/j.1365-2311.2010.01233.x
Morales, J., Chiu, H., Oo, T., Plaza, R., Hoskins, S., & Govind, S. (2005). Biogenesis, structure, and immune-suppressive effects of virus-like particles of a Drosophila parasitoid, Leptopilina victoriae. Journal of Insect Physiology, 51(2), 181–195. https://doi.org/10.1016/j.jinsphys.2004.11.002
Moreau, S. J. M., Cherqui, A., Doury, G., Dubois, F., Fourdrain, Y., Sabatier, L., Bulet, P., Saarela, J., Prévost, G., & Giordanengo, P. (2004). Identification of an aspartylglucosaminidase-like protein in the venom of the parasitic wasp Asobara tabida (hymenoptera: Braconidae). Insect Biochemistry and Molecular Biology, 34(5), 485–492. https://doi.org/10.1016/j.ibmb.2004.03.001
Mortimer, N. T. (2013). Parasitoid wasp virulence: A window into fly immunity. Fly, 7(4), 242–248. https://doi.org/10.4161/fly.26484
Mouton, L. (2004). Diversité et densité bactériennes dans les symbioses à infections multiples: Régulation et effets sur l'hôte, cas des associations Wolbachia-insectes. Université Claude Bernard-Lyon, 1.
Mouton, L., Henri, H., Bouletreau, M., & Vavre, F. (2003). Strain-specific regulation of intracellular Wolbachia density in multiply infected insects. Molecular Ecology, 12(12), 3459–3465. https://doi.org/10.1046/j.1365-294X.2003.02015.x
Mouton, L., Henri, H., Boulétreau, M., & Vavre, F. (2005). Multiple infections and diversity of cytoplasmic incompatibility in a haplodiploid species. Heredity, 94(2), 187–192. https://doi.org/10.1038/sj.hdy.6800596
Mouton, L., Henri, H., Charif, D., Boulétreau, M., & Vavre, F. (2007). Interaction between host genotype and environmental conditions affects bacterial density in Wolbachia symbiosis. Biological Letters, 3(2), 210–213. https://doi.org/10.1098/rsbl.2006.0590
Mouton, L., Henri, H., & Fleury, F. (2009). Interactions between coexisting intracellular genomes: Mitochondrial density and Wolbachia infection. Applied Environmental Microbiology, 75(7), 1916–1921. https://doi.org/10.1128/AEM.02677-08
Muller, D., Giron, D., Desouhant, E., Rey, B., Casas, J., Lefrique, N., & Visser, B. (2017). Maternal age affects offspring nutrient dynamics. Journal of Insect Physiology, 101, 123–131. https://doi.org/10.1016/j.jinsphys.2017.07.011
Nappi, A. J. (1970). Defense reactions of Drosophila euronotus larvae against the Hymenopterous parasite Pseudeucoila bochei. Journal of Invertebrate Pathology, 16, 408–418. https://doi.org/10.1016/0022-2011(70)90160-6
Nappi, A. J. (1975). Cellular immune reactions of larvae of Drosophila algonquin. Parasitology, 70, 189–194. https://doi.org/10.1017/S0031182000049659
Nappi, A. J. (2010). Cellular immunity and pathogen strategies in combative interactions involving Drosophila hosts and their endoparasitic wasps. Invertebrate Survival Journal, 7(2), 198–210.
Nappi, A. J., & Silvers, M. (1984). Cell surface changes associated with cellular immune reactions in Drosophila. Science, 225, 1166–1168. https://doi.org/10.1126/science.6433482
Nappi, A. J., & Streams, F. A. (1969). Haemocytic reactions of Drosophila melanogaster to the parasites Pseudocoila mellipes and P. bochei. Journal of Insect Physiology, 15(9), 1551–1566. https://doi.org/10.1016/0022-1910(69)90175-9
Nomano, F. Y., Kasuya, N., Matsuura, A., Suwito, A., Mitsui, H., Buffington, M. L., & Kimura, M. T. (2017). Genetic differentiation of Ganaspis brasiliensis (hymenoptera: Figitidae) from east and Southeast Asia. Applied Entomological Zoology, 52, 429–437. https://doi.org/10.1007/s13355-017-0493-0
Nordlander, G. (1980). Revision of the genus Leptopilina Förster, 1869, with notes on the status of some other genera (hymenoptera, Cynipoidea: Eucoilidae). Insect Systematics and Evolution, 11(4), 428–453. https://doi.org/10.1163/187631280794710024
Novkovic, B., Mitsui, H., Suwito, A., & Kimura, M. T. (2011). Taxonomy and phylogeny of Leptopilina species (hymenoptera: Cynipoidea: Figitidae) attacking frugivorous drosophilid flies in Japan, with description of three new species. Entomological Science, 14(3), 333–346. https://doi.org/10.1111/j.1479-8298.2011.00459.x
O'Grady, P. M., & DeSalle, R. (2018). Phylogeny of the genus Drosophila. Genetics, 209(1), 1–25. https://doi.org/10.1534/genetics.117.300583
Papaj, D. R., Snellen, H., Swaans, K., & Vet, L. E. M. (1994). Unrewarding experiences and their effect on foraging in the parasitic wasp Leptopilina heterotoma (hymenoptera: Eucoilidae). Journal of Insect Behaviour, 7(4), 465–481. https://doi.org/10.1007/BF02025444
Papaj, D. R., & Vet, L. E. M. (1990). Odor learning and foraging success in the parasitoid, Leptopilina heterotoma. Journal of Chemical Ecology, 16(11), 3137–3150. https://doi.org/10.1007/BF00979616
Paredes, J. C., Herren, J. K., Schüpfer, F., & Lemaitre, B. (2016). The role of lipid competition for endosymbiont-mediated protection against parasitoid wasps in Drosophila. mBio, 7(4), 1–8. https://doi.org/10.1128/mBio.01006-16
Patot, S., Allemand, R., Fleury, F., & Varaldi, J. (2012). An inherited virus influences the coexistence of parasitoid species through behaviour manipulation: A symbiont mediates interspecific competition. Ecology Letters, 15(6), 603–610. https://doi.org/10.1111/j.1461-0248.2012.01774.x
Pfeiffer, L., Ruther, J., Hofferberth, J., & Stökl, J. (2018). Interference of chemical defence and sexual communication can shape the evolution of chemical signals. Scientific Reports, 8(1), 321. https://doi.org/10.1038/s41598-017-18376-w
Pierce, G. J., & Ollason, J. G. (1987). Eight reasons why optimal foraging theory is a complete waste of time. Oikos, 49(1), 111–117. https://doi.org/10.2307/3565560
Poirié, M., Carton, Y., & Dubuffet, A. (2009). Virulence strategies in parasitoid hymenoptera as an example of adaptive diversity. Comptes Rendus Biologies, 332(2–3), 311–320. https://doi.org/10.1016/j.crvi.2008.09.004
Poirié, M., Colinet, D., & Gatti, J.-L. (2014). Insights into function and evolution of parasitoid wasp venoms. Current Opinion in Insect Science, 6, 52–60. https://doi.org/10.1016/j.cois.2014.10.004
Pompanon, F., Fouillet, P., & Bouletreau, M. (1995). Emergence rhythms and protandry in relation to daily patterns of locomotor activity in Trichogramma species. Evolutionary Ecology, 9(5), 467–477. https://doi.org/10.1007/bf01237829
Poyet, M., Havard, S., Prevost, G., Chabrerie, O., Doury, G., Gibert, P., & Eslin, P. (2013). Resistance of Drosophila suzukii to the larval parasitoids Leptopilina heterotoma and Asobara japonica is related to haemocyte load. Physiological Entomology, 38(1), 45–53. https://doi.org/10.1111/phen.12002
Poyet, M., Le Roux, V., Gibert, P., Meirland, A., Prévost, G., Eslin, P., & Chabrerie, O. (2015). The wide potential trophic niche of the asiatic fruit fly Drosophila suzukii: The key of its invasion success in temperate Europe? PLoS ONE, 10(11), e0142785. https://doi.org/10.1371/journal.pone.0142785
Price, P. W. (1974). Strategies for egg production. Evolution, 28(1), 76–84. https://doi.org/10.1111/j.1558-5646.1974.tb00728.x
Ramroop, J. R., Heavner, M. E., Razzak, Z. H., & Govind, S. (2021). A parasitoid wasp of Drosophila employs preemptive and reactive strategies to deplete its host's blood cells. PLoS Pathogens, 17(5), e1009615. https://doi.org/10.1371/journal.ppat.1009615
Raychoudhury, R., & Werren, J. H. (2012). Host genotype changes bidirectional to unidirectional cytoplasmic incompatibility in Nasonia longicornis. Heredity, 108(p), 105–114. https://doi.org/10.1038/hdy.2011.53
Renou, M. (2014). Chapter 2: Pheromones and general odor perception in insects. In C. Mucignat-Caretta (Ed.), Neurobiology of chemical communication. CRC Press/Taylor & Francis.
Ridley, M. (1988). Mating frequency and fecundity in insects. Biological Reviews, 63(4), 509–549. https://doi.org/10.1111/j.1469-185X.1988.tb00669.x
Ridley, M. (1993). Clutch size and mating frequency in parasitic hymenoptera. The American Naturalist, 142, 893–910. https://doi.org/10.1086/285579
Ris, N., Allemand, R., Fouillet, P., & Fleury, F. (2004). The joint effect of temperature and host species induce complex genotype-by-environment interactions in the larval parasitoid of Drosophila, Leptopilina heterotoma (hymenoptera: Figitidae). Oikos, 106(3), 451–456. https://doi.org/10.1111/j.0030-1299.2004.13274.x
Rizki, R. M., & Rizki, T. M. (1991). Effects of lamellolysin from a parasitoid wasp on Drosophila blood cells in vitro. Journal of Experimental Zoology, 257(2), 236–244. https://doi.org/10.1002/jez.1402570214
Rizki, T. M., Rizki, R. M., & Carton, Y. (1990). Leptopilina heterotoma and L. boulardi: Strategies to avoid cellular defense responses of Drosophila melanogaster. Experimental Parasitology, 70(4), 466–475. https://doi.org/10.1016/0014-4894(90)90131-U
Roff, D. A. (2001). Life history, evolution. Encyclopedia of Biodiversity, 4, 631–641. https://doi.org/10.1016/B978-0-12-384719-5.00087-3
Roitberg, B. D., Mangel, M., Lalonde, R. G., Roitberg, C. A., van Alphen, J. J. M., & Vet, L. (1992). Seasonal dynamic shifts in patch exploitation by parasitic wasps. Behavioral Ecology, 3(2), 156–165. https://doi.org/10.1093/beheco/3.2.156
Ronquist, F. (1995). Phylogeny and early evolution of the Cynipoidea (hymenoptera). Systematic Entomology, 205(4), 309–335. https://doi.org/10.1111/j.1365-3113.1995.tb00099.x
Ronquist, F. (1999). Phylogeny, classification and evolution of the Cynipoidea. Zoologica Scripta, 28(1–2), 139–164. https://doi.org/10.1046/j.1463-6409.1999.00022.x
Rossi Stacconi, M. V., Buffington, M., Daane, K. M., Dalton, D. T., Grassi, A., Kaçar, G., Miller, B., Miller, J. C., Baser, N., Ioriatti, C., Walton, V. M., Wiman, N. G., Wang, X., & Anfora, G. (2015). Host stage preference, efficacy and fecundity of parasitoids attacking Drosophila suzukii in newly invaded areas. Biological Control, 84, 28–35. https://doi.org/10.1016/j.biocontrol.2015.02.003
Rossi Stacconi, M. V., Panel, A., Baser, N., Ioriatti, C., Pantezzi, T., & Anfora, G. (2017). Comparative life history traits of indigenous Italian parasitoids of Drosophila suzukii and their effectiveness at different temperatures. Biological Control, 112, 20–27. https://doi.org/10.1016/j.biocontrol.2017.06.003
Rouault, J. (1979). Rôle des parasites entomophages dans la compétition entre espèces jumelles de Drosophiles. Comptes Rendus de l'Académies des Sciences Paris, 289, 643–646.
Ruschioni, S., van Loon, J. J. A., Smid, H. M., & van Lenteren, J. C. (2015). Insects can count: Sensory basis of host discrimination in parasitoid wasps revealed. PLoS ONE, 10(10), e0138045. https://doi.org/10.1371/journal.pone.0138045
Samson-Boshuizen, M., Bakker, K., & van Lenteren, J. C. (1974). Success of parasitization of Pseudeucoila bochei weld (Hym., Cynip.): A matter of experience. Netherlands Journal of Zoology, 24(1), 67–85. https://doi.org/10.1163/002829674X00174
Schlenke, T. A., Morales, J., Govind, S., & Clark, A. G. (2007). Contrasting infection strategies in generalist and specialist wasp parasitoids of Drosophila melanogaster. PLoS Pathogens, 3, 1486–1501. https://doi.org/10.1371/journal.ppat.0030158
Seehausen, L. M., Ris, N., Driss, L., Racca, A., Girod, P., Warot, S., Borowiec, N., Toševski, I., & Kenis, M. (2020). Evidence for a cryptic parasitoid species reveals its suitability as a biological control agent. Scientific Reports, 10(1), 19096. https://doi.org/10.1038/s41598-020-76180-5
Shropshire, J. D., Leigh, B., & Bordenstein, S. R. (2020). Symbiont-mediated cytoplasmic incompatibility: What have we learned in 50 years? eLife, 9, e61989. https://doi.org/10.7554/eLife.61989
Simons, M. T. T. P., Suverkropp, B. P., Vet, L. E. M., & Moed, G. (1992). Comparison of learning in related generalist and specialist eucoilid parasitoids. Entomologia Experimentalis et Applicata, 64(2), 117–124. https://doi.org/10.1111/j.1570-7458.1992.tb01601.x
Sinclair, B. J., & Marshall, K. E. (2018). The many roles of fats in overwintering insects. Journal of Experimental Biology, 221(Suppl_1), jeb161836. https://doi.org/10.1242/jeb.161836
Siva-Jothy, M. T., Moret, Y., & Rolff, J. (2005). Insect immunity: An evolutionary ecology perspective. Advances in Insect Physiology, 32, 1–48. https://doi.org/10.1016/s0065-2806(05)32001-7
Sobhy, I. S., Goelen, T., Herrera-Malaver, B., Verstrepen, K. J., Wäckers, F., Jacquemyn, H., & Lievens, B. (2019). Associative learning and memory retention of nectar yeast volatiles in a generalist parasitoid. Animal Behaviour, 153, 137–146. https://doi.org/10.1016/j.anbehav.2019.05.006
Stökl, J., & Herzner, G. (2016). Morphology and ultrastructure of the allomone and sex-pheromone producing mandibular gland of the parasitoid wasp Leptopilina heterotoma (hymenoptera: Figitidae). Arthropod Structure & Development, 45(4), 333–340. https://doi.org/10.1016/j.asd.2016.06.003
Stökl, J., Hofferberth, J., Pritschet, M., Brummer, M., & Ruther, J. (2012). Stereoselective chemical defense in the Drosophila parasitoid Leptopilina heterotoma is mediated by (−)-Iridomyrmecin and (+)-Isoiridomyrmecin. Journal of Chemical Ecology, 38(4), 331–339. https://doi.org/10.1007/s10886-012-0103-0
Stökl, J., Machacek, Z., & Ruther, J. (2015). Behavioural flexibility of the chemical defence in the parasitoid wasp Leptopilina heterotoma. The Science of Nature, 102(11–12), 67. https://doi.org/10.1007/s00114-015-1317-0
Stökl, J., & Steiger, S. (2017). Evolutionary origin of insect pheromones. Current Opinion in Insect Science, 24, 36–42. https://doi.org/10.1016/j.cois.2017.09.004
Streams, F. A. (1968). Defense reactions of Drosophila species (Diptera: Drosophilidae) to the parasite Pseudeucoila bochei (hymenoptera: Cynipidae). Annals of the Entomological Society of America, 61(1), 158–164. https://doi.org/10.1093/aesa/61.1.158
van Strien-van Liempt, W. T. F. H. (1983). The competition between Asobara tabida Nees von Esenbeck, 1834 and Leptopilina Heterotoma (Thomson, 1862) in multiparasitized hosts. Netherlands Journal of Zoology, 33(2), 125–163. https://doi.org/10.1163/002829683X00066
van Strien-van Liempt, W. T. F. H., & van Alphen, J. J. M. (1981). The absence of interspecific host discrimination in Asobara tabida Nees and Leptopilina heterotoma (Thomson), coexisting larval parasitoids of Drosophila species. Netherlands Journal of Zoology, 31(4), 701–712. https://doi.org/10.1163/002829681X00239
Struck, T. H., Feder, J. L., Bendiksby, M., Birkeland, S., Cerca, J., Gusarov, V. I., Kistenich, S., Larsson, K.-H., Liow, L. H., Nowak, M. D., Stedje, B., Bachmann, L., & Dimitrov, D. (2018). Finding evolutionary processes hidden in cryptic species. Trends in Ecology and Evolution, 33(3), 153–163. https://doi.org/10.1016/j.tree.2017.11.007
Sunday, J. M., Bates, A. E., & Dulvy, N. K. (2012). Thermal tolerance and the global redistribution of animals. Nature Climate Change, 2, 686–690. https://doi.org/10.1038/nclimate1539
Ugur, B., Chen, K., & Bellen, H. J. (2016). Drosophila tools and assays for the study of human diseases. Disease Models & Mechanisms, 9(3), 235–244. https://doi.org/10.1242/dmm.023762
van Alphen, J. J. M., Eebes, H., van Lenteren, J. C., & Nell, H. W. (1984). The response of a polyphagous parasitoid (Leptopilina heterotoma (Thomson)) to a kairomone produced by one of its hosts (Drosophila melanogaster Meigen). Netherlands Journal of Zoology, 34(2), 215–219. https://doi.org/10.1163/002829684X00164
van Alphen, J. J. M., & Janssen, A. R. M. (1982). Host selection by Asobara tabida Nees (Braconidae; Alysiinae) a larval parasitoid of fruit inhabiting Drosophila species. Netherlands Journal of Zoology, 32(2), 215–231. https://doi.org/10.5281/zenodo.805740
van Alphen, J. J. M., & Thunnissen, I. (1983). Host selection and sex allocation by Pachycrepoideus vindemiae Rondani (Pteromalidae) as a facultative hyperparasitoid of Asobara tabida Nees (Braconidae; Alysiinae) and Leptopilina heterotoma (Cynipoidea; Eucoilidae). Netherlands Journal of Zoology, 33(4), 497–514. https://doi.org/10.1163/002829683X00228
van Alphen, J. J. M., van Dijken, M. J., & Waage, J. K. (1987). A functional approach to superparasitism: Host discrimination needs not be learnt by. Netherlands Journal of Zoology, 37(2), 167–179. https://doi.org/10.1163/002829686X00045
van Alphen, J. J. M., & Vet, L. (1986). An evolutionary approach to host finding and selection. In J. K. Waage & D. J. Greathead (Eds.), Insect parasitoids (pp. 23–61). Academic Press.
van Alphen, J. J. M., & Visser, M. E. (1990). Superparasitism as an adaptive strategy for insect parasitoids. Annual Review of Entomology, 35, 59–79. https://doi.org/10.1146/annurev.en.35.010190.000423
van Batenburg, F. H. D., Bakker, K., van Lenteren, J. C., & van Alphen, J. J. M. (1983). Searching for and parasitization of larvae of Drosophila melanogaster (Dipt.: Drosophilidae) by Leptopilina heterotoma (Hym.: Eucoilidae): A Monte Carlo simulation model and the real situation. Netherlands Journal of Zoology, 33(3), 306–336. https://doi.org/10.1163/002829683X00156
van den Assem, J. (1969). Reproductive behaviour of Pseudeucoila bochei (hymenoptera: Cynipidae). Netherlands Journal of Zoology, 19(4), 641–648. https://doi.org/10.1163/002829669X00080
van der Hoeven, R., & Vet, L. E. M. (1984). Comparison of the behavioural response of two Leptopilina species (hymenoptera: Eucoilidae), living in different microhabitats, to kairomone of their host (Drosophilidae). Netherlands Journal of Zoology, 34(2), 220–227. https://doi.org/10.1163/002829684X00173
van Lenteren, J. C. (1972). Contact-chemoreceptors on the ovipositor of Pseudeucoila bochei Weld (Cynipidae). Netherlands Journal of Zoology, 22(3), 347–350. https://doi.org/10.1163/002829672X00158
van Lenteren, J. C. (1976). The development of host discrimination and the prevention of superparasitism in the parasite Pseudeucoila bochei Weld (Hym.: Cynipidae). Netherlands Journal of Zoology, 26(1), 1–83. https://doi.org/10.1163/002829676X00055
van Lenteren, J. C. (1991). Encounters with parasitized hosts: To leave or not to leave a patch. Netherlands Journal of Zoology, 41(2–3), 144–157. https://doi.org/10.1163/156854291X00090
van Lenteren, J. C., & Bakker, K. (1975). Discrimination between parasitised and unparasitised hosts in the parasitic wasp Pseudeucoila bochei: A matter of learning. Nature, 254(5499), 417–419. https://doi.org/10.1038/254417a0
van Lenteren, J. C., & Bakker, K. (1978). Behavioural aspects of the functional responses of a parasite (Pseudeucoila Bochei Weld) to its host (Drosophila melanogaster). Netherlands Journal of Zoology, 28(2), 213–233. https://doi.org/10.1163/002829678X00062
van Lenteren, J. C., Isidoro, N., & Bin, F. (1998). Functional anatomy of the ovipositor clip in the parasitoid Leptopilina heterotoma (Thompson) (hymenoptera: Eucoilidae), a structure to grip escaping host larvae. International Journal of Insect Morphology and Embryology, 27(3), 263–268. https://doi.org/10.1016/S0020-7322(98)00019-1
van Lenteren, J. C., Ruschioni, S., Romani, R., van Loon, J. J. A., Qiu, Y. T., Smid, H. M., Isidoro, N., & Bin, F. (2007). Structure and electrophysiological responses of gustatory organs on the ovipositor of the parasitoid Leptopilina heterotoma. Arthropod Structure & Development, 36(3), 271–276. https://doi.org/10.1016/j.asd.2007.02.001
Varaldi, J., Fouillet, P., Boulétreau, M., & Fleury, F. (2005). Superparasitism acceptance and patch-leaving mechanisms in parasitoids: A comparison between two sympatric wasps. Animal Behaviour, 69(6), 1227–1234. https://doi.org/10.1016/j.anbehav.2004.09.012
Vavre, F., Dedeine, F., Quillon, M., Fouillet, P., Fleury, F., & Boulétreau, M. (2001). Within-species diversity of Wolbachia-induced cytoplasmic incompatibility in haplodiploid insects. Evolution, 55(8), 1710–1714. https://doi.org/10.1111/j.0014-3820.2001.tb00691.x
Vavre, F., Fleury, F., Lepetit, D., Fouillet, P., & Bouletreau, M. (1999). Phylogenetic evidence for horizontal transmission of Wolbachia in host-parasitoid associations. Molecular Biology and Evolution, 16(12), 1711–1723. https://doi.org/10.1093/oxfordjournals.molbev.a026084
Vavre, F., Fleury, F., Varaldi, J., Fouillet, P., & Bouleatreau, M. (2000). Evidence for female mortality in Wolbachia-mediated cytoplasmic incompatibility in haplodiploid insects: Epidemiologic and evolutionary consequences. Evolution, 54(1), 191–200. https://doi.org/10.1111/j.0014-3820.2000.tb00019.x
Vayssade, C., Martel, V., Moiroux, J., Fauvergue, X., van Alphen, J. J. M., & van Baaren, J. (2012). The response of life-history traits to a new species in the community: A story of Drosophila parasitoids from the Rhône and Saône valleys: Shift of life-history trade-off. Biological Journal of the Linnean Society, 107(1), 153–165. https://doi.org/10.1111/j.1095-8312.2012.01918.x
Veerkamp, F. A. (1982). Genetic variation in the pattern of initial oviposition behaviour of Leptopilina heterotoma Thomson (=Pseudeucoila bochei weld), a parasite of Drosophila melanogaster. Netherlands Journal of Zoology, 32(1), 88–107. https://doi.org/10.1163/002829682X00067
Vet, L. E. M., & Bakker, K. (1985). A comparative functional approach to the host detection behaviour of parasitic wasps. 2. A quantitative study on eight eucoilid species. Oikos, 44(3), 487–498. https://doi.org/10.2307/3565790
Vet, L. E. M., De Jong, A. G., Franchi, E., & Papaj, D. R. (1998). The effect of complete versus incomplete information on odour discrimination in a parasitic wasp. Animal Behaviour, 55(5), 1271–1279. https://doi.org/10.1006/anbe.1997.0686
Vet, L. E. M., & Groenewold, A. W. (1990). Semiochemicals and learning in parasitoids. Journal of Chemical Entomology, 16(11), 3119–3135. https://doi.org/10.1007/BF00979615
Vet, L. E. M., Janse, C., van Achterberg, C., & van Alphen, J. J. M. (1984). Microhabitat location and niche segregation in two sibling species of Drosophilid parasitoids: Asobara tabida (Nees) and A. rufescens (Foerster) (Braconidae: Alysiinae). Oecologia, 61(2), 182–188. https://doi.org/10.1007/BF00396757
Vet, L. E. M., & Papaj, D. R. (1992). Effects of experience on parasitoid movement in odour plumes. Physiological Entomology, 17(1), 90–96. https://doi.org/10.1111/j.1365-3032.1992.tb00994.x
Vet, L. E. M., & Schoonman, G. (1988). The influence of previous foraging experience on microhabitat acceptance in Leptopilina heterotoma. Journal of Insect behaviour, 1(4), 387–392. https://doi.org/10.1007/BF01054501
Vet, L. E. M., Sokolowski, M. B., MacDonald, D. E., & Snellen, H. (1993). Responses of a generalist and a specialist parasitoid (hymenoptera: Eucoilidae) to Drosophilid larval kairomones. Journal of Insect Behaviour, 6(5), 615–624. https://doi.org/10.1007/BF01048127
Vet, L. E. M., & van Opzeeland, K. (1985). Olfactory microhabitat selection in Leptopilina heterotoma (Thomson) (Hym.: Eucoilidae), a parasitoid of Drosophilidae. Netherlands Journal of Zoology, 35(3), 497–504. https://doi.org/10.1163/002829685X00352
Visser, B., Alborn, H. T., Rondeaux, S., Haillot, M., Hance, T., Rebar, D., Riederer, J. M., Tiso, S., van Eldijk, T. J. B., Weissing, F. J., & Nieberding, C. M. (2021). Phenotypic plasticity explains apparent reverse evolution of fat synthesis in parasitic wasps. Scientific Reports, 11, 7751. https://doi.org/10.1038/s41598-021-86736-8
Visser, B., & Ellers, J. (2008). Lack of lipogenesis in parasitoids: A review of physiological mechanisms and evolutionary implications. Journal of Insect Physiology, 54(9), 1315–1322. https://doi.org/10.1016/j.jinsphys.2008.07.014
Visser, B., Hance, T., Noël, C., Pels, C., Kimura, M. T., Stökl, J., Geuverink, E., & Nieberding, C. M. (2018). Variation in lipid synthesis, but genetic homogeneity, among Leptopilina parasitic wasp populations. Ecology and Evolution, 8, 7355–7364. https://doi.org/10.1002/ece3.4265
Visser, B., Le Lann, C., den Blanken, F. J., Harvey, J. A., van Alphen, J. J. M., & Ellers, J. (2010). Loss of lipid synthesis as an evolutionary consequence of a parasitic lifestyle. Proceedings of the National Academy of Sciences of the United States of America, 107(19), 8677–8682. https://doi.org/10.1073/pnas.1001744107
Visser, B., Le Lann, C., Nieberding, C. M., Lammers, M., Hahn, D. A., Alborn, H. T., Enriquez, T., Scheifler, M., Harvey, J. A., & Ellers, J. (2022). Why do many parasitoids lack adult triglyceride accumulation, despite functioning fatty acid biosynthesis machinery? EcoEvoRxiv. https://doi.org/10.32942/osf.io/zpf4j
Visser, B., Le Lann, C., Snaas, H., Hardy, I., & Harvey, J. (2014). Consequences of resource competition for sex allocation and discriminative behaviors in a hyperparasitoid wasp. Behavioral Ecology and Sociobiology, 68, 105–113. https://doi.org/10.1007/s00265-013-1627-1
Visser, B., Roelofs, D., Hahn, D. A., Teal, P. E. A., Mariën, J., & Ellers, J. (2012). Transcriptional changes associated with lack of lipid synthesis in parasitoids. Genome Biology and Evolution, 4(8), 864–874. https://doi.org/10.1093/gbe/evs065
Visser, M. E. (1993). Adaptive self- and conspecific superparasitism in the solitary parasitoid Leptopilina heterotoma (hymenoptera: Eucoilidae). Behavioral Ecology, 4(1), 22–28. https://doi.org/10.1093/beheco/4.1.22
Visser, M. E. (1995). The effect of competition on oviposition decisions of Leptopilina heterotoma (hymenoptera: Eucoilidae). Animal Behaviour, 49(6), 1677–1687. https://doi.org/10.1016/0003-3472(95)90089-6(6)
Visser, M. E., Luyckx, B., Nell, H. W., & Boskamp, G. J. F. (1992). Adaptive superparasitism in solitary parasitoids: Marking of parasitized hosts in relation to the pay-off from superparasitism. Ecological Entomology, 17(1), 76–82. https://doi.org/10.1111/j.1365-2311.1992.tb01042.x
Visser, M. E., van Alpen, J. J. M., & Nell, H. K. (1990). Adaptive superparasitism and patch time allocation in solitary parasitoids: the influence of the number of parasitoids depleting patch. Behaviour, 114(164), 23–35.
Visser, M. E., van Alphen, J. J. M., & Nell, H. W. (1992). Adaptive superparasitism and patch time allocation in solitary parasitoids: The influence of pre-patch experience. Behavioural Ecology and Sociobiology, 31(3), 163–171. https://doi.org/10.1007/BF00168643
Vuarin, P., Allemand, R., Moiroux, J., van Baaren, J., & Gibert, P. (2012). Geographic variations of life history traits and potential trade-offs in different populations of the parasitoid Leptopilina heterotoma. Naturwissenschaften, 99(11), 903–912. https://doi.org/10.1007/s00114-012-0972-7
Wachi, N., Nomano, F. Y., Mitsui, H., Kasuya, N., & Kimura, M. T. (2015). Taxonomy and evolution of putative thelytokous species of Leptopilina (hymenoptera: Figitidae) from Japan, with description of two new species: Thelytokous Leptopilina wasps from Japan. Entomological Science, 18(1), 41–54. https://doi.org/10.1111/ens.12089
Wältermann, M., & Steinbüchel, A. (2005). Neutral lipid bodies in prokaryotes: Recent insights into structure, formation, and relationship to eukaryotic lipid depots. Journal of Bacteriology, 187(11), 3607–3619. https://doi.org/10.1128/JB.187.11.3607-3619.2005
Wang, S., Wang, L., Liu, J., Zhang, D., & Liu, T. (2021). Multiple mating of Aphelinus asychis enhance the number of female progeny but shorten the longevity. Insects, 12(9), 823. https://doi.org/10.3390/insects12090823
Weiss, I., Hofferberth, J., Ruther, J., & Stökl, J. (2015). Varying importance of cuticular hydrocarbons and iridoids in the species-specific mate recognition pheromones of three closely related Leptopilina species. Frontiers in Ecology and Evolution, 3, 19. https://doi.org/10.3389/fevo.2015.00019
Weiss, I., Rössler, T., Hofferberth, J., Brummer, M., Ruther, J., & Stökl, J. (2013). A nonspecific defensive compound evolves into a competition avoidance cue and a female sex pheromone. Nature Communications, 4, 2767. https://doi.org/10.1038/ncomms3767
Weiss, I., Ruther, J., & Stökl, J. (2015). Species specificity of the putative male antennal aphrodisiac pheromone in Leptopilina heterotoma, Leptopilina boulardi, and Leptopilina victoriae. BioMed Research International, 2015, 202965. https://doi.org/10.1155/2015/202965
Weld, L. H. (1944). Description of new Cynipidae including two new genera (hymenoptera). Proceedings of the Entomological Society of Washington, 46(p), 55–66.
Werren, J. (2009). Larval RNAi in Nasonia (parasitoid wasp). Cold Spring Harbor Protocols, 2009(10), 1–6. https://doi.org/10.1101/pdb.prot5311
Werren, J. H., Windsor, D., & Guo, L. (1995). Distribution of Wolbachia among neotropical arthropods. Proceedings of the Royal Society of London, 262(1364), 197–204. https://doi.org/10.1098/rspb.1995.0196
Wertheim, B. (2022). Adaptations and counter-adaptations in Drosophila host-parasitoid interactions: Advances in the molecular mechanisms. Current Opinion in Insect Science, 51, 100896. https://doi.org/10.1016/j.cois.2022.100896
Wertheim, B., Allemand, R., Vet, L. E. M., & Dicke, M. (2006). Effects of aggregation pheromone on individual behaviour and food web interactions: A field study on Drosophila. Ecological Entomology, 31(3), 216–226. https://doi.org/10.1111/j.1365-2311.2006.00757.x
Wertheim, B., Vet, L. E. M., & Dicke, M. (2003). Increased risk of parasitism as ecological costs of using aggregation pheromones: Laboratory and field study of Drosophila-Leptopilina interaction. Oikos, 100(2), 269–282. https://doi.org/10.1034/j.1600-0706.2003.11579.x
Wey, B., Heavner, M. E., Wittmeyer, K. T., Briese, T., Hopper, K. R., & Govind, S. (2020). Immune suppressive extracellular vesicle proteins of Leptopilina heterotoma are encoded in the wasp genome. G3, 10(1), 1–12. https://doi.org/10.1534/g3.119.400349
Wiskerke, J. S. C., Dicke, M., & Vet, L. E. M. (1993). Larval parasitoid uses aggregation pheromone of adult hosts in foraging behaviour: A solution to the reliability-detectability problem. Oecologia, 93(1), 145–148. https://doi.org/10.1007/BF00321204
Wyatt, T. D. (2010). Pheromones and signature mixtures: Defining species-wide signals and variable cues for identity in both invertebrates and vertebrates. Journal of Comparative Physiology A, 196(10), 685–700. https://doi.org/10.1007/s00359-010-0564-y
Wyatt, T. D. (2014). Pheromones and animal behavior: Chemical signals and signature mixtures. Cambridge University Press. https://doi.org/10.1017/CBO9781139030748
Xie, J., Butler, S., Sanchez, G., & Mateos, M. (2014). Male killing Spiroplasma protects Drosophila melanogaster against two parasitoid wasps. Heredity, 112(4), 399–408. https://doi.org/10.1038/hdy.2013.118
Xie, J., Tiner, B., Vilchez, I., & Mateos, M. (2011). Effect of the Drosophila endosymbiont Spiroplasma on parasitoid wasp development and on the reproductive fitness of wasp-attacked fly survivors. Evolutionary Ecology, 25(5), 1065–1079. https://doi.org/10.1007/s10682-010-9453-7
Xie, J., Vilchez, I., & Mateos, M. (2010). Spiroplasma bacteria enhance survival of Drosophila hydei attacked by the parasitic wasp Leptopilina heterotoma. PLoS ONE, 5(8), e12149. https://doi.org/10.1371/journal.pone.0012149
Yang, L., Qiu, L., Fang, Q., Stanley, D. W., & Ye, G. (2020). Cellular and humoral immune interactions between Drosophila and its parasitoids. Insect Sci., 28(5), 1208–1227. https://doi.org/10.1111/1744-7917.12863
Zhang, S., Qian, B., Ilyas, A., Gong, X., Xu, J., Liu, P., & Hu, H. (2022). Influence of parasitoid states on the propensity to enter and the stay in a patch. Journal of Insect Behaviour, 35, 56–64. https://doi.org/10.1007/s10905-022-09799-z
Zhou, W., Rousset, F., & O'Neill, S. (1998). Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proceedings of the Royal Society of London, 265(1395), 509–515. https://doi.org/10.1098/rspb.1998.0324
