Herbivorous insects can escape the strong pressure of parasitoids by switching to feeding on new host plants. Parasitoids can adapt to this change but at the cost of changing their preferences and performance. For gregarious parasitoids, fitness changes are not always observable in the F1 generation but only in the F2 generation. Here, with the model species and gregarious parasitoid Anaphes flavipes, we examined fitness changes in the F1 generation under pressure from the simulation of host switching, and by a new two-generation approach, we determined the impact of these changes on fitness in the F2 generation. We showed that the parasitoid preference for host plants depends on hatched or oviposited learning in relation to the possibility of parasitoid decisions between different host plants. Interestingly, we showed that after simulation of parasitoids following host switching, in the new environment of a fictitious host plant, parasitoids reduced the fictitious host. At the same time, parasitoids also reduced fertility because in fictitious hosts, they are not able to complete larval development. However, from a two-generation approach, the distribution of parasitoid offspring into both native and fictitious hosts caused lower parasitoid clutch size in native hosts and higher individual offspring fertility in the F2 generation.

Crop Research Institute Drnovská 507 161 06 Praha 6 Ruzyně Czech Republic

Department of Plant Protection Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Kamýcká 129 165 00 Prague 6 Suchdol Czech Republic

Department of Zoology Faculty of Science Charles University Viničná 7 128 43 Prague 2 Czech Republic

Institute of Entomology Biological Centre Czech Academy of Sciences Branišovská 31 370 05 České Budějovice Czech Republic

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Hairston NG, Smith FE, Lawrence BS. Community structure, population control, and competition. Am. Nat. 1960;94:421–425. doi: 10.1086/282146. DOI

Gross P. Insect behavioral and morphological defenses against parasitoid. Annu. Rev. Entomol. 1993;38:251–273. doi: 10.1146/annurev.en.38.010193.001343. DOI

Tylikinais JM, Tscharntke T, Klein AM. Diversity, ecosystem function and stability of parasitoid—host interactions across a tropical habitat gradient. Ecology. 2006;87:3047–3057. doi: 10.1890/0012-9658(2006)87[3047:DEFASO]2.0.CO;2. PubMed DOI

Strand MR, Obrycki JJ. Host specificity of insect parasitoids and predators. Bioscience. 1996;46:422–429. doi: 10.2307/1312876. DOI

Dawkins R, Krebs JR. Arms races between and within species. Proc. R. Soc. Lond. B. 1979;205:489–511. doi: 10.1098/rspb.1979.0081. PubMed DOI

Kraaijeveld AR, van Alphen JJM, Godfray HCJ. The coevolution of host resistance and parasitoid virulence. Parasitology. 1998;116:29–45. doi: 10.1017/S0031182000084924. PubMed DOI

Jeffries MJ, Lawton JH. Enemy free space and the structure of ecological communities. Biol. J. Linn. Soc. 1984;23:269–286. doi: 10.1111/j.1095-8312.1984.tb00145.x. DOI

Grosman AH, Molina-Rugama AJ, Mendes-Dias R, Sabelis MW, Menken SBJ, et al. No adaptation of a herbivore to a novel host but loss of adaptation to its native host. Sci. Rep.-UK. 2015;5:16211. doi: 10.1038/srep16211. PubMed DOI PMC

Diamond SE, Kingsolver JG. Fitness consequences of host plant choice: A field experiment. Oikos. 2010;119:542–550. doi: 10.1111/j.1600-0706.2009.17242.x. DOI

Meijer K, Schilthuizen M, Beukeboom L, Smit C. A review and meta-analysis of the enemy release hypothesis in plant–herbivorous insect systems. PeerJ. 2016;4:e2778. doi: 10.7717/peerj.2778. PubMed DOI PMC

Forbes AA, Powell TH, Stelinski LL, Smith JJ, Feder JL. Sequential sympatric speciation across trophic levels. Science. 2009;323:776–779. doi: 10.1126/science.1166981. PubMed DOI

Grosman AH, Holtz AM, Pallini A, Sabelis MW, Janssen A. Parasitoids follow herbivorous insects to a novel host plant, generalist predators less so. Entomol. Exp. Appl. 2017;162:261–271. doi: 10.1111/eea.12545. DOI

Soler R, Bezemer TM, Van Der Putten WH, Vet LE, Harvey JA. Root herbivore effects on above-ground herbivore, parasitoid and hyperparasitoid performance via changes in plant quality. J. Anim. Ecol. 2005;74:1121–1130. doi: 10.1111/j.1365-2656.2005.01006.x. DOI

Ode PJ. Plant chemistry and natural enemy fitness: Effects on herbivore and natural enemy interactions. Annu. Rev. Entomol. 2006;51:163–185. doi: 10.1146/annurev.ento.51.110104.151110. PubMed DOI

Thompson JN. Trade-offs in larval performance on normal and novel hosts. Entomol. Exp. Appl. 1996;80:133–139. doi: 10.1111/j.1570-7458.1996.tb00903.x. DOI

Lucas É, Coderre D, Brodeur J. Intraguild predation among aphid predators: Characterization and influence of extraguild prey density. Ecology. 1998;79:1084–1092. doi: 10.1890/0012-9658(1998)079[1084:IPAAPC]2.0.CO;2. DOI

Henry LM, May N, Acheampong S, Gillespie DR, Roitberg BD. Host-adapted parasitoids in biological control: Does source matter? Ecol. Appl. 2010;20:242–250. doi: 10.1890/08-1869.1. PubMed DOI

Mackauer M. Sexual size dimorphism in solitary parasitoid wasps: influence of host quality. Oikos. 1996;76:265–272. doi: 10.2307/3546199. DOI

Bezemer TM, Mills NJ. Clutch size decisions of a gregarious parasitoid under laboratory and feld conditions. Anim. Behav. 2003;66:1119–1128. doi: 10.1006/anbe.2003.2296. DOI

Samková A, Hadrava J, Skuhrovec J, Janšta P. Host population density and presence of predators as key factors influencing the number of gregarious parasitoid Anaphes flavipes offspring. Sci. Rep.-UK. 2019;9:6081. doi: 10.1038/s41598-019-42503-4. PubMed DOI PMC

Schmidt JM, Smith JJB. Correlations between body angles and substrate curvature in the parasitoid wasp Trichogramma minutum: a possible mechanism of host radius measurement. J. Exp. Biol. 1986;125:271–285. doi: 10.1242/jeb.125.1.271. DOI

Boivin G, Baaren J. The role of larval aggression and mobility in the transition between solitary and gregarious development in parasitoid wasps. Ecol. Lett. 2000;3:469–474. doi: 10.1046/j.1461-0248.2000.00174.x. DOI

Mayhew PJ. The evolution of gregariousness in parasitoid wasps. P. Roy. Soc. Lond. B. Bio. 1998;265:383–389. doi: 10.1098/rspb.1998.0306. DOI

Pexton JJ, Mayhew PJ. Competitive interactions between parasitoid larvae and the evolution of gregarious development. Oecologia. 2004;141:179–190. doi: 10.1007/s00442-004-1659-3. PubMed DOI

Harvey PH, Partridge L. Murderous mandibles and black holes in hymenopteran wasps. Nature. 1987;326:128–129. doi: 10.1038/326128a0. DOI

Godfray HCJ. The evolution of clutch size in parasitic wasps. Am. Nat. 1987;129:221–233. doi: 10.1086/284632. DOI

Rosenheim JA. Single-sex broods and the evolution of nonsiblicidal parasitoid wasps. Am. Nat. 1993;141:90–104. doi: 10.1086/285462. DOI

Mayhew PJ, van Alphen JJ. Gregarious development in alysiine parasitoids evolved through a reduction in larval aggression. Anim. Behav. 1999;58:131–141. doi: 10.1006/anbe.1999.1106. PubMed DOI

Pexton JJ, Mayhew PJ. Immobility: The key to family harmony? Trends. Ecol. Evol. 2001;16:7–9. doi: 10.1016/S0169-5347(00)02034-6. PubMed DOI

Hamilton WD. Extraordinary sex ratios. Science. 1967;156:477–488. doi: 10.1126/science.156.3774.477. PubMed DOI

Mayhew PJ, Hardy IC. Nonsiblicidal behavior and the evolution of clutch size in bethylid wasps. Am. Nat. 1998;151:409–424. doi: 10.1086/286129. PubMed DOI

Zaviezo T, Mills N. Factors influencing the evolution of clutch size in a gregarious insect parasitoid. J. Anim. Ecol. 2000;69:1047–1057. doi: 10.1046/j.1365-2656.2000.00460.x. DOI

Koppik M, Tiel A, Hofmeister TS. Adaptive decision making or diferential mortality: What causes ofspring emergence in a gregarious parasitoid? Entomol. Exp. Appl. 2014;150:208–216. doi: 10.1111/eea.12154. DOI

Visser ME, Van Alphen JJ, Hemerik L. Adaptive superparasitism and patch time allocation in solitary parasitoids: An ESS model. J. Anim. Ecol. 1992;61:93–101. doi: 10.2307/5512. DOI

Waage JK, Ming NS. The reproductive strategy of a parasitic wasp: I. optimal progeny and sex allocation in Trichogramma evanescens. J. An. Ecol. 1984;53:401–415. doi: 10.2307/4524. DOI

Harvey JA, Poelman EH, Tanaka T. Intrinsic inter-and intraspecific competition in parasitoid wasps. Ann. Rev. Entomol. 2013;58:333–351. doi: 10.1146/annurev-ento-120811-153622. PubMed DOI

Harvey JA, Bezemer TM, Gols R, Nakamatsu Y, Tanaka T. Comparing the physiological effects and function of larval feeding in closely-related endoparasitoids (Braconidae: Microgastrinae) Physiol. Entomol. 2008;33:217–225. doi: 10.1111/j.1365-3032.2008.00623.x. DOI

Cloutier C, Duperron J, Tertuliano M, McNeil JN. Host instar, body size and fitness in the koinobiotic parasitoid Aphidius nigripes. Entomol. Exp. Appl. 2000;97:29–40. doi: 10.1046/j.1570-7458.2000.00713.x. DOI

Bai B, Luck RF, Forster L, Stephens B, Janssen JM. The effect of host size on quality attributes of the egg parasitoid Trichogramma pretiosum. Entomol. Exp. Appl. 1992;64:37–48. doi: 10.1111/j.1570-7458.1992.tb01592.x. DOI

Kazmer DJ, Luck RF. Field tests of the size-fitness hypothesis in the egg parasitoid Trichogramma Pretiosum. Ecology. 1995;76:412–425. doi: 10.2307/1941200. DOI

Samková A, Hadrava J, Skuhrovec J, Janšta P. Reproductive strategy as a major factor determining female body size and fertility of a gregarious parasitoid. J. Appl. Entomol. 2019;143:441–450. doi: 10.1111/jen.12615. DOI

Wei K, Tang YL, Wang XY, Cao LM, Yang ZQ. The developmental strategies and related profitability of an idiobiont ectoparasitoid Sclerodermus pupariae vary with host size. Ecol. Entomol. 2014;39:101–108. doi: 10.1111/een.12074. DOI

May RM, Hassell MP, Anderson MR, Tonkyn DV. Density dependence in host-parasitoid models. J. Anim. Ecol. 1981;50:855–865. doi: 10.2307/4142. DOI

Hoddle MS, Van Driesche RG, Elkinton JS, Sanderson JP. Discovery and utilization of Bemisia argentifolii patches by Eretmocerus eremicus and Encarsia formosa (Beltsville strain) in greenhouses. Entomol. Exp. Appl. 1998;87:15–28. doi: 10.1046/j.1570-7458.1998.00300.x. DOI

Samková A, Raska J, Hadrava J, Skuhrovec J. An intergenerational approach for prediction of parasitoid population dynamics. BioRxiv. 2021 doi: 10.1101/2021.02.22.432341. DOI

Anderson RC, Paschke JD. The biology and ecology of Anaphes flavipes (Hymenoptera: Mymaridae), an exotic egg parasite of the cereal leaf beetle. Ann. Entomol. Soc. Am. 1968;61:1–5. doi: 10.1093/aesa/61.1.1. DOI

Klomp H, Teerink BJ. The significance of oviposition rates in the egg parasite Trichogramma embryophagum Htg. Arch. Neerl. Zool. 1967;17:350–375. doi: 10.1163/036551667X00065. DOI

Waage JK, Lane JA. The reproductive strategy of a parasitic wasp: II. Sex allocation and local mate competition in Trichogramma evanescens. J. Anim. Ecol. 1984;53:417–426. doi: 10.2307/4525. DOI

Dysart RJ, Maltby HL, Brunson MH. Larval parasites of Oulema melanopus in Europe and their colonization in the United States. Entomophaga. 1973;18:133–167. doi: 10.1007/BF02372026. DOI

Skuhrovec J, Douda O, Zouhar M, Maňasová M, Nový P, Božik M, Klouček P. Insecticidal activity of two formulations of essential oils against the cereal leaf beetle. Acta Agr. Scand. 2018;68:489–495.

Jervis MA, Ellers J, Harvey JA. Resource acquisition, allocation, and utilization in parasitoid reproductive strategies. Annu. Rev. Entomol. 2008;53:361–385. doi: 10.1146/annurev.ento.53.103106.093433. PubMed DOI

Vinson SB, Iwantsch GF. Host suitability for insect parasitoids. Ann. Rev. Entomol. 1980;25:397–419. doi: 10.1146/annurev.en.25.010180.002145. DOI

Mackauer M, Sequeira R, Otto M. Vertical Food Web Interactions. Springer; 1997. Growth and development in parasitoid wasps adaptation to variable host resources; pp. 191–203.

Ode PJ. Plant toxins and parasitoid trophic ecology. Curr. Opin. Insect sci. 2019;32:118–123. doi: 10.1016/j.cois.2019.01.007. PubMed DOI

Cronin JT, Abrahamson WG. Do parasitoids diversify in response to host-plant shifts by herbivorous insects? Ecol. Entomol. 2001;26:347–355. doi: 10.1046/j.1365-2311.2001.00332.x. DOI

Sarfraz M, Dosdall LM, Keddie BA. Host plant nutritional quality affects the performance of the parasitoid Diadegma insulare. Biol. Control. 2009;51:34–41. doi: 10.1016/j.biocontrol.2009.07.004. DOI

Harvey JA. Factors affecting the evolution of development strategies in parasitoid wasps: The importance of functional constraints and incorporating complexity. Entomol. Exp. Appl. 2005;117:1–13. doi: 10.1111/j.1570-7458.2005.00348.x. DOI

Cortesero AM, Monge JP. Influence of pre-emergence experience on response to host and host plant odours in the larval parasitoid Eupelmus vuilleti. Entomol. Exp. Appl. 1994;72:281–288. doi: 10.1111/j.1570-7458.1994.tb01828.x. DOI

Gandolfi M, Mattiacci L, Dorn S. Preimaginal learning determines adult response to chemical stimuli in a parasitic wasp. Proc. Roy. Soc. Lon. Series. B-Biol. Scien. 2003;270:2623–2629. doi: 10.1098/rspb.2003.2541. PubMed DOI PMC

Kester KM, Barbosa P. Postemergence learning in the insect parasitoid, Cotesia congregata (Say) (Hymenoptera: Braconidae) J. Insect Behav. 1991;4:727–742. doi: 10.1007/BF01052227. DOI

Vet LE, Groenewold AW. Semiochemicals and learning in parasitoids. J. Chem. Ecol. 1990;16:3119–3135. doi: 10.1007/BF00979615. PubMed DOI

Samková A, Hadrava J, Skuhrovec J, Janšta P. Effect of adult feeding and timing of host exposure on the fertility and longevity of the parasitoid Anaphes flavipes. Entomol. Exp. Appl. 2019;167:932–938. doi: 10.1111/eea.12843. DOI

Jervis MA, Heimpel GE, Ferns PN, Harvey JA, Kidd NA. Life-history strategies in parasitoid wasps: A comparative analysis of ‘ovigeny’. J. Anim. Ecol. 2001;70:442–458. doi: 10.1046/j.1365-2656.2001.00507.x. DOI

Bjorksten TA, Hoffmann AA. Persistence of experience effects in the parasitoid Trichogramma nr. brassicae. Ecol. Entomol. 1998;23:110–117. doi: 10.1046/j.1365-2311.1998.00120.x. DOI

Lentz AJ, Kester KM. Postemergence experience affects sex ratio allocation in a gregarious insect parasitoid. J. Insect. Behav. 2008;21:34–45. doi: 10.1007/s10905-007-9102-3. DOI

Nishida R. Sequestration of defensive substances from plants by Lepidoptera. Annu. Rev. Entomol. 2002;47:57–92. doi: 10.1146/annurev.ento.47.091201.145121. PubMed DOI

Zvereva EL, Rank NE. Fly parasitoid Megaselia opacicornis uses defensive secretions of the leaf beetle Chrysomela lapponica to locate its host. Oecologia. 2004;140:516–522. doi: 10.1007/s00442-004-1602-7. PubMed DOI

Roy HE, Handley LJL, Schönrogge K, Poland RL, Purse BV. Can the enemy release hypothesis explain the success of invasive alien predators and parasitoids? Biocontrol. 2011;56:451–468. doi: 10.1007/s10526-011-9349-7. DOI

Snyder WE, Ives AR. Interactions between specialist and generalist natural enemies: Parasitoids, predators, and pea aphid biocontrol. Ecology. 2003;84:91–107. doi: 10.1890/0012-9658(2003)084[0091:IBSAGN]2.0.CO;2. DOI

Polis GA, Myers CA, Holt RD. The ecology and evolution of intraguild predation: Potential competitors that eat each other. Annu. Rev. Ecol. Syst. 1989;20:297–330. doi: 10.1146/annurev.es.20.110189.001501. DOI

Nakashima Y, Senoo N. Avoidance of ladybird trails by an aphid parasitoid Aphidius ervi: active period and efects of prior oviposition experience. Entomol. Exp. Appl. 2003;109:163–166. doi: 10.1046/j.1570-7458.2003.00094.x. DOI

Samková A, Raška J, Hadrava J, Skuhrovec J, Janšta P. Female manipulation of offspring sex ratio in the gregarious parasitoid Anaphes flavipes from a new two-generation approach. BioRxiv. 2021 doi: 10.1101/2021.02.22.432331. DOI

Visser ME. The importance of being large: the relationship between size and fitness in females of the parasitoid Aphaereta minuta (Hymenoptera: Braconidae) J. Anim. Ecol. 1994;63:963–978. doi: 10.2307/5273. DOI

Banks M, Thomson DJ. Lifetime mating success in the damselfly Coenagrion puella. Anim. Behav. 1985;33:1175–1183. doi: 10.1016/S0003-3472(85)80178-0. DOI

Ellers J, Jervis M. Body size and the timing of egg production in parasitoid wasps. Oikos. 2003;102:164–172. doi: 10.1034/j.1600-0706.2003.12285.x. DOI

Anderson RC, Paschke JD. Additional Observations on the Biology of Anaphes flavipes (Hymenoptera: Mymaridae), with Special Reference to the Efects of Temperature and Superparasitism on Development. Ann. Entomol. Soc. Am. 1969;62:1316–1321. doi: 10.1093/aesa/62.6.1316. DOI

Bezděk J, Baselga A. Revision of western Palaearctic species of the Oulema melanopus group, with description of two new species from Europe (Coleoptera: Chrysomelidae: Criocerinae) Acta. Ent. Mus. Nat. Pra. 2015;55:273–304.

R. Core Team R . A language and environment for statistical computing. R Foundation for Statistical Computing. R Core Team; 2020.

Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting Linear Mixed-Effects Models Using lme4. J. Stat. Softw67, 1–48. (2015) URL: https://CRAN.R-project.org/package=Hmisc.

Harrell, F. E. Jr, Dupont, C., et mult. al. (2020) Hmisc: Harrell Miscellaneous. R package version 4.4–2. URL: https://CRAN.R-project.org/package=Hmisc.

Signorell et mult. al. (2021). DescTools: Tools for descriptive statistics. R package version 0.99.40. URL: https://cran.r-project.org/package=DescTools.

Genetic analysis reveals conspecificity of two nominal species of Anaphes fairyflies (Hymenoptera: Mymaridae), egg parasitoids of Oulema leaf beetle (Coleoptera: Chrysomelidae) pests of cereal crops in Europe and of rice in East Asia