Bet-hedging; Fitness; Fluctuating; Global warming; Insects; Plasticity
Abstract :
[en] The Earth's climate is changing at a rapid pace. To survive in increasingly fluctuating and unpredictable environments, species can either migrate or evolve through rapid local adaptation, plasticity and/ or bet-hedging. For small ectotherm insects, like parasitoids and their hosts, phenotypic plasticity and bet-hedging could be critical strategies for population and species persistence in response to immediate, intense and unpredictable temperature changes. Here, we focus on studies evaluating phenotypic responses to variable predictable thermal conditions (for which phenotypic plasticity is favoured) and unpredictable thermal environments (for which bethedging is favoured), both within and between host and parasitoid generations. We then address the effects of fluctuating temperatures on host-parasitoid interactions, potential cascading effects on the food web, as well as biological control services. We conclude our review by proposing a road map for designing experiments to assess if plasticity and bet-hedging can be adaptive strategies, and to disentangle how fluctuating temperatures can affect the evolution of these two strategies in parasitoids and their hosts.
Disciplines :
Zoology
Author, co-author :
Le Lann, Cećile; UMR 6553, Universitéde Rennes, CNRS, ECOBIO (ećosystemes, biodiversite, Rennes, France
Van Baaren, Joan; UMR 6553, Universitéde Rennes, CNRS, ECOBIO (ećosystemes, biodiversite, Rennes, France
Visser, Bertanne ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs ; Evolution and Ecophysiology Group, Biodiversity Research Centre, Earth and Life Institute, UCLouvain, Louvain-la-Neuve, Belgium
Language :
English
Title :
Dealing with predictable and unpredictable temperatures in a climate change context: the case of parasitoids and their hosts
Abram, P. K., Boivin, G., Moiroux, J. and Brodeur, J. (2017). Behavioural effects of temperature on ectothermic animals: unifying thermal physiology and behavioural plasticity. Biol. Rev. 92, 1859-1876. doi:10.1111/brv.12312
Alford, L., Androdias, A., Franco, T., Pierre, J. S., Burel, F. and Van Baaren, J. (2016). Potential host manipulation by the aphid parasitoid Aphidius avenae to enhance cold tolerance. PLOS One 11, 1-14. doi:10.1371/journal.pone.0168693
Alford, L., Tougeron, K., Pierre, J. S., Burel, F. and van Baaren, J. (2018). The effect of landscape complexity and microclimate on the thermal tolerance of a pest insect. Insect Sci. 25, 905-915. doi:10.1111/1744-7917.12460
Amat, I., Van Alphen, J. J. M., Kacelnik, A., Desouhant, E. and Bernstein, C. (2017). Adaptations to different habitats in sexual and asexual populations of parasitoid wasps: a meta-analysis. PeerJ 2017, 1-27. doi:10.7717/peerj.3699
Andrade, T. O., Krespi, L., Bonnardot, V., van Baaren, J. and Outreman, Y. (2016). Impact of change in winter strategy of one parasitoid species on the diversity and function of a guild of parasitoids. Oecologia 180, 877-888. doi:10. 1007/s00442-015-3502-4
Bahar, M. H., Hegedus, D., Soroka, J., Coutu, C., Bekkaoui, D. and Dosdall, L. (2013). Survival and Hsp70 gene expression in Plutella xylostella and its larval parasitoid Diadegma insulare varied between slowly ramping and abrupt extreme temperature regimes. PLOS One 8, 1-9. doi:10.1371/journal.pone.0073901
Bannerman, J. A. and Roitberg, B. D. (2014). Impact of extreme and fluctuating temperatures on aphid-parasitoid dynamics. Oikos 123, 89-98. doi:10.1111/j. 1600-0706.2013.00686.x Barrett, R. D. H. and Schluter, D. (2008). Adaptation from standing genetic variation. Trends Ecol. Evol. 23, 38-44. doi:10.1016/j.tree.2007.09.008
Bathiany, S., Scheffer, M., Van Nes, E. H., Williamson, M. S. and Lenton, T. M. (2018). Abrupt climate change in an oscillating world. Sci. Rep. 8, 1-12. doi:10. 1038/s41598-018-23377-4
Beaumont, H. J. E., Gallie, J., Kost, C., Ferguson, G. C. and Rainey, P. B. (2009). Experimental evolution of bet hedging. Nature 462, 90-93. doi:10.1038/ nature08504
Biale, H., Geden, C. J., Chiel, E. and Fryxell, R. T. (2020). Heat adaptation of the house fly (Diptera: Muscidae) and its associated parasitoids in Israel. J. Med. Entomol. 57, 113-121. doi:10.1093/jme/tjz152
Blanford, S., Thomas, M. B., Pugh, C. and Pell, J. K. (2003). Temperature checks the RedQueen? Resistance and virulence in a fluctuating environment. Ecol. Lett. 6, 2-5. doi:10.1046/j.1461-0248.2003.00387.x
Boivin, G. (1994). Overwintering strategies of egg parasitoids. In Biological Control with Egg Parasitoids (ed. E. Wajnberg and S. A. Hassan), pp. 219-244. CAB International.
Brockerhoff, E. G. and Kenis, M. (1997). Oviposition, life cycle, and parasitoids of the spruce cone maggot, Strobilomyia anthracina (Diptera: Anthomyiidae), in the Alps. Entomol. Res. 87, 555-562. doi:10.1017/S0007485300038645
Brodeur, J. and McNeil, J. N. (1989). Seasonal microhabitat selection by an endoparasitoid through adaptive modification of host behavior. Science 244, 226-228. doi:10.1126/science.244.4901.226
Burdick, S. C., Prischmann-Voldseth, D. A. and Harmon, J. P. (2015). Density and distribution of soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae) in response to UV radiation. Popul. Ecol. 57, 457-466. doi:10.1007/ s10144-015-0501-6
Burgess, S. C. and Marshall, D. J. (2014). Adaptive parental effects: the importance of estimating environmental predictability and offspring fitness appropriately. Oikos 123, 769-776. doi:10.1111/oik.01235
Castellanos, N. L., Bueno, A. F., Haddi, K., Silveira, E. C., Rodrigues, H. S., Hirose, E., Smagghe, G. and Oliveira, E. E. (2019). The fitness and economic benefits of rearing the parasitoid Telenomus podisi under fluctuating temperature regime. Neotrop. Entomol. 48, 934-948. doi:10.1007/s13744-019-00717-1
Cavieres, G., Alruiz, J. M., Medina, N. R., Bogdanovich, J. M. and Bozinovic, F. (2019). Transgenerational and within-generation plasticity shape thermal performance curves. Ecol. Evol. 9, 2072-2082. doi:10.1002/ece3.4900
Chihrane, J., Lauge?, G. and Hawlitzky, N. (1993). Effects of high temperature shocks on the development and biology of Trichogramma brassicae [Hym.: Trichogrammatidae]. Entomophaga 38, 185-192. doi:10.1007/BF02372552
Co? nsoli, F. L. and Parra, J. R. P. (1995). Effects pf constant and alternating temperatures on Trichogramma galloi Zucchi (Hem., Trichogrammatidae) biology II. - parasitism capacity and longevity. J. Appl. Entomol. 119, 667-670. doi:10. 1111/j.1439-0418.1995.tb01355.x
Corley, J. C., Capurro, A. F. and Bernstein, C. (2004). Prolonged diapause and the stability of host-parasitoid interactions. Theor. Popul. Biol. 65, 193-203. doi:10. 1016/j.tpb.2003.09.005
Dahlgaard, J., Loeschcke, V., Michalak, P. and Justesen, J. (1998). Induced thermotolerance and associated expression of the heat-shock protein Hsp70 in adult Drosophila melanogaster. Funct. Ecol. 12, 786-793. doi:10.1046/j.1365- 2435.1998.00246.x
Danks, H. V. (1987). Insect Dormancy: An Ecological Perspective. Ottawa: Biological Survey of Canada (Terrestrial Arthropods).
Dedryver, C. A., Hulle?, M., Le Gallic, J. F., Caillaud, M. C. and Simon, J. C. (2001). Coexistence in space and time of sexual and asexual populations of the cereal aphid Sitobion avenae. Oecologia 128, 379-388. doi:10.1007/ s004420100674
Delava, E., Fleury, F. and Gibert, P. (2016). Effects of daily fluctuating temperatures on the Drosophila-Leptopilina boulardi parasitoid association. J. Therm. Biol. 60, 95-102. doi:10.1016/j.jtherbio.2016.06.012
Donelson, J. M., Salinas, S., Munday, P. L. and Shama, L. N. S. (2018). Transgenerational plasticity and climate change experiments: where do we go from here? Glob. Chang. Biol. 24, 13-34. doi:10.1111/gcb.13903
Donelson, J. M., Wong, M., Booth, D. J. and Munday, P. L. (2016). Transgenerational plasticity of reproduction depends on rate of warming across generations. Evol. Appl. 9, 1072-1081. doi:10.1111/eva.12386
Easterling, D. R., Meehl, G. A., Parmesan, C., Changnon, S. A., Karl, T. R. and Mearns, L. O. (2000). Climate extremes: observations, modeling, and impacts. Science 289, 2068-2074. doi:10.1126/science.289.5487.2068
Ellers, J., Kiers, T., Currie, C. R., Mcdonald, B. R. and Visser, B. (2012). Ecological interactions drive evolutionary loss of traits. Ecol. Lett. 15, 1071-1082. doi:10.1111/j.1461-0248.2012.01830.x
Eoche-Bosy, D., Outreman, Y., Andrade, T. O., Krespi, L. and van Baaren, J. (2016). Seasonal variations of host resources influence foraging strategy in parasitoids. Entomol. Exp. Appl. 161, 11-19. doi:10.1111/eea.12494
Feder, M. E. and Hofmann, G. E. (1999). Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu. Rev. Physiol. 61, 243-282. doi:10.1146/annurev.physiol.61.1.243
Furlong, M. J. and Zalucki, M. P. (2017). Climate change and biological control: the consequences of increasing temperatures on host-parasitoid interactions. Curr. Opin. Insect Sci. 20, 39-44. doi:10.1016/j.cois.2017.03.006
Gerber, N. and Kokko, H. (2018). Abandoning the ship using sex, dispersal or dormancy: multiple escape routes from challenging conditions. Phil. Trans. R. Soc. 373, B37320170424. doi:10.1098/rstb.2017.0424
Ghalambor, C. K., Hoke, K. L., Ruell, E. W., Fischer, E. K., Reznick, D. N. and Hughes, K. A. (2015). Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature. Nature 525, 372-375. doi:10.1038/ nature15256
Ghalambor, C. K., McKay, J. K., Carroll, S. P. and Reznick, D. N. (2007). Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct. Ecol. 21, 394-407. doi:10.1111/j.1365- 2435.2007.01283.x
Gienapp, P., Lof, M., Reed, T. E., McNamara, J., Verhulst, S. and Visser, M. E. (2013). Predicting demographically sustainable rates of adaptation: can great tit breeding time keep pace with climate change? Philos. Trans. R. Soc. B Biol. Sci. 368, 20120289. doi:10.1098/rstb.2012.0289
Godfray, H. C. J. (1994). Parasitoids: Behavioural and Evolutionary Ecology. West Sussex: Princeton University Press.
Grigaltchik, V. S.,Ward, A. J.W. and Seebacher, F. (2012). Thermal acclimation of interactions: differential responses to temperature change alter predator-prey relationship. Proc. R. Soc. B Biol. Sci. 279, 4058-4064. doi:10.1098/rspb.2012. 1277
Haaland, T. R., Wright, J. and Ratikainen, I. I. (2019). Bet-hedging across generations can affect the evolution of variance-sensitive strategies within generations. Proc. R. Soc. B Biol. Sci. 286, 20192070. doi:10.1098/rspb.2019. 2070
Halkett, F., Harrington, R., Hulle?, M., Kindlmann, P., Menu, F., Rispe, C. and Plantegenest, M. (2004). Dynamics of production of sexual forms in aphids: theoretical and experimental evidence for adaptive 'coin-flipping' plasticity. Am. Nat. 163. doi:10.1086/383618
Hance, T., van Baaren, J., Vernon, P. and Boivin, G. (2007). Impact of extreme temperatures on parasitoids in a climate change perspective. Annu. Rev. Entomol. 52, 107-126. doi:10.1146/annurev.ento.52.110405.091333
He, X. Z., Wang, Q., Walker, J. T. S., Rogers, D. J. and Lo, P. L. (2010). A sophisticated life history strategy in a parasitoid wasp: producing univoltine and multivoltine phenotypes in a local population. Biol. Control 54, 276-284. doi:10. 1016/j.biocontrol.2010.05.014
Hegland, S. J., Nielsen, A., La?zaro, A., Bjerknes, A. L. and Totland, . (2009). How does climate warming affect plant-pollinator interactions? Ecol. Lett. 12, 184-195. doi:10.1111/j.1461-0248.2008.01269.x
Hoffmann, A. A., S rensen, J. G. and Loeschcke, V. (2003). Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. J. Therm. Biol. 28, 175-216. doi:10.1016/S0306-4565(02)00057-8
Hopper, K. R. (1999). Risk-spreading and bet-hedging in insect population biology. Annu. Rev. Entomol. 44, 535-560. doi:10.1146/annurev.ento.44.1.535
Hulle, M., Coeur d'Acier, A., Bankhead-Dronnet, S. and Harrington, R. (2010). Aphids in the face of global changes. Comptes Rendus Biol. 333, 497-503. doi:10. 1016/j.crvi.2010.03.005
Iltis, C., Moreau, J., Manie?re, C., Thie?ry, D., Delbac, L. and Loua? pre, P. (2020). Where you come from matters: temperature influences host-parasitoid interaction through parental effects. Oecologia 192, 853-863. doi:10.1007/s00442-020- 04613-z
IPCC (2014). Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (ed. R. Pachauri and L. Meyer), 151pp. Geneva, Switzerland: IPCC. ISBN: 978-92-9169-143-2.
Ismaeil, I., Doury, G., Desouhant, E., Dubois, F., Prevost, G. and Couty, A. (2013). Trans-generational effects of mild heat stress on the life history traits of an aphid parasitoid. PLOS One 8, 1-9. doi:10.1371/journal.pone.0054306
Jackson, S., Nielsen, D. M. and Singh, N. D. (2015). Increased exposure to acute thermal stress is associated with a non-linear increase in recombination frequency and an independent linear decrease in fitness in Drosophila. BMC Evol. Biol. 15, 1-8. doi:10.1186/s12862-015-0452-8
Jeffs, C. T. and Lewis, O. T. (2013). Effects of climate warming on host-parasitoid interactions. Ecol. Entomol. 38, 209-218. doi:10.1111/een.12026
Jervis, M. A. (ed.) (2005). Insects as Natural Enemies: A Practical Perspective. Springer.
Joschinski, J. and Bonte, D. (2020). Transgenerational plasticity and bet-hedging: a framework for reaction norm evolution. Front. Ecol. Evol. 8, 1-12. doi:10.3389/ fevo.2020.517183
Josso, C., Moiroux, J., Vernon, P., Van Baaren, J. and Van Alphen, J. J. M. (2011). Temperature and parasitism by Asobara tabida (Hymenoptera: Braconidae) influence larval pupation behaviour in two Drosophila species. Naturwissenschaften 98, 705-709. doi:10.1007/s00114-011-0813-0
Karunakar, P., Bhalla, A. and Sharma, A. (2019). Transgenerational inheritance of cold temperature response in Drosophila. FEBS Lett. 593, 594-600. doi:10.1002/ 1873-3468.13343
Kraaijeveld, A., Nowee, B. and Najem, R. W. (1995). Adaptive variation in hostselection behaviour of Asobara tabida, a parasitoid of Drosophila larvae. Funct. Ecol. 9, 113-118. doi:10.2307/2390097
Krebs, R. A. and Loeschcke, V. (1994). Effects of exposure to short-term heat stress on fitness components in Drosophila melanogaster. J. Evol. Biol. 7, 39-49. doi:10.1046/j.1420-9101.1994.7010039.x
Krespi, L., Dedryver, C. A., Rabasse, J. M. and Ne?non, J.-P. (1994). A morphometric comparison of aphid mummies containing diapausing vs. nondiapausing larvae of Aphidius rhopalosiphi (Hymenoptera: Braconidae, Aphidiinae). Bull. Entomol. Res. 84, 45-50. doi:10.1017/S0007485300032211
Kristensen, T. N., Hoffmann, A. A., Overgaard, J., S rensen, J. G., Hallas, R. and Loeschcke, V. (2008). Costs and benefits of cold acclimation in fieldreleased Drosophila. Proc. Natl. Acad. Sci. USA 105, 216-221. doi:10.1073/pnas. 0708074105
Kristensen, T. N., Ketola, T. and Kronholm, I. (2020). Adaptation to environmental stress at different timescales. Ann. N. Y. Acad. Sci. 1476, 5-12. doi:10.1111/nyas. 13974
Kwon, Y., Shim, H.-S., Wang, X. and Montell, C. (2008). Control of thermotactic behavior via coupling of a TRP channel to a phospholipase C signaling cascade. Nat. Neurosci. Neurosci. 11, 871-873. doi:10.1038/nn.2170
Lacoume, S., Bressac, C. and Chevrier, C. (2007). Sperm production and mating potential of males after a cold shock on pupae of the parasitoid wasp Dinarmus basalis (Hymenoptera: Pteromalidae). J. Insect Physiol. 53, 1008-1015. doi:10. 1016/j.jinsphys.2007.05.006
Lagos, N. A., Fuentes-Contreras, E., Bozinovic, F. and Niemeyer, H. M. (2001). Behavioural thermoregulation in Acyrthosiphon pisum (Homoptera: Aphididae): the effect of parasitism by Aphidius ervi (Hymenoptera: Braconidae). J. Therm. Biol. 26, 133-137. doi:10.1016/S0306-4565(00)00033-4
Le Lann, C., Lodi, M. and Ellers, J. (2014). Thermal change alters the outcome of behavioural interactions between antagonistic partners. Ecol. Entomol. 39, 578-588. doi:10.1111/een.12135
Lenton, T. M., Dakos, V., Bathiany, S. and Scheffer, M. (2017). Observed trends in the magnitude and persistence of monthly temperature variability. Sci. Rep. 7, 1-10. doi:10.1038/s41598-017-06382-x
Liu, L., Yermolaieva, O., Johnson,W. A., Abboud, F. M. andWelsh, M. J. (2003). Identification and function of thermosensory neurons in Drosophila larvae. Nat. Neurosci. 6, 267-273. doi:10.1038/nn1009
Lockwood, B. L., Julick, C. R. and Montooth, K. L. (2017). Maternal loading of a small heat shock protein increases embryo thermal tolerance in Drosophila melanogaster. J. Exp. Biol. 220, 4492-4501. doi:10.1242/jeb.164848
Logan, M. L. and Cox, C. L. (2020). Genetic Constraints, Transcriptome Plasticity, and the Evolutionary Response to Climate Change. Frontiers in Genetics 11. doi:10.3389/fgene.2020.538226
Machekano, H., Mvumi, B. M. and Nyamukondiwa, C. (2018). Loss of coevolved basal and plastic responses to temperature may underlie trophic level host- parasitoid interactions under global change. Biol. Control 118, 44-54. doi:10.1016/ j.biocontrol.2017.12.005
Mahdjoub, T. and Menu, F. (2008). Prolonged diapause: a trait increasing invasion speed? J. Theor. Biol. 251, 317-330. doi:10.1016/j.jtbi.2007.12.002
Marshall, D. J. and Uller, T. (2007). When is a maternal effect adaptive? Oikos 116, 1957-1963. doi:10.1111/j.2007.0030-1299.16203.x
De Meester, L., Stoks, R. and Brans, K. I. (2018). Genetic adaptation as a biological buffer against climate change: potential and limitations. Integr. Zool. 13, 372-391. doi:10.1111/1749-4877.12298
Memmott, J., Craze, P. G., Waser, N. M. and Price, M. V. (2007). Global warming and the disruption of plant-pollinator interactions. Ecol. Lett. 10, 710-717. doi:10. 1111/j.1461-0248.2007.01061.x
Menu, F. and Desouhant, E. (2002). Bet-hedging for variability in life cycle duration: bigger and later-emerging chestnut weevils have increased probability of a prolonged diapause. Oecologia 132, 167-174. doi:10.1007/s00442-002-0969-6
Menu, F., Roebuck, J.-P. and Viala, M. (2000). Bet-hedging diapause strategies in stochastic environments. Am. Nat. 155, 724-734. doi:10.1086/303355
Moiroux, J., Delava, E., Fleury, F. and Van Baaren, J. (2013). Local adaptation of a Drosophila parasitoid: habitat-specific differences in thermal reaction norms. J. Evol. Biol. 26, 1108-1116. doi:10.1111/jeb.12122
Mutamiswa, R., Chidawanyika, F. and Nyamukondiwa, C. (2018). Thermal plasticity potentially mediates the interaction between host Chilo partellus Swinhoe (Lepidoptera: Crambidae) and endoparasitoid Cotesia flavipes Cameron (Hymenoptera: Braconidae) in rapidly changing environments. Pest Manag. Sci. 74, 1335-1345. doi:10.1002/ps.4807
Olofsson, H., Ripa, J. and Jonze?n, N. (2009). Bet-hedging as an evolutionary game: the trade-off between egg size and number. Proc. R. Soc. B Biol. Sci. 276, 2963-2969. doi:10.1098/rspb.2009.0500
Pandey, M. and Singh, B. (1993). Effect of biotic and abiotic factors on pupation height in four species of Drosophila. Indian J. Exp. Biol. 31, 912-917.
Parmesan, C. (2006). Ecological and evolutionary responses to recent climate change. Annu. Rev. 37, 637-669. doi:10.1146/annurev.ecolsys.37.091305.110100
Parmesan, C. and Yohe, G. (2003). A globally coherent fingerprint of climate change. Nature 421, 37-42. doi:10.1038/nature01286
Peng, X., Zhao, Q., Guo, X., Su, S., Liu, L., Li, Y., Song, C. and Chen, M. (2020). Effects of variable maternal temperature on offspring development and reproduction of Rhopalosiphum padi, a serious global pest of wheat. Ecol. Entomol. 45, 269-277. doi:10.1111/een.12796
Perez, M. F. and Lehner, B. (2019). Intergenerational and transgenerational epigenetic inheritance in animals. Nat. Cell Biol. 21, 143-151. doi:10.1038/ s41556-018-0242-9
Philippi, T. and Seger, J. (1989). Hedging one's evolutionary bets, revisited. Trends Ecol. Evol. 4, 41-44. doi:10.1016/0169-5347(89)90138-9
Pigliucci, M. (2005). Evolution of phenotypic plasticity: where are we going now? Trends Ecol. Evol. 20, 481-486. doi:10.1016/j.tree.2005.06.001
Rajon, E., Desouhant, E., Chevalier, M., De?bias, F. and Menu, F. (2014). The evolution of bet hedging in response to local ecological conditions. Am. Nat. 184, E1-E15. doi:10.1086/676506
Reitz, S. R. and Nettles, W. C., Jr. (1994). Regulation of Helicoverpa zea larval behavior by the parasitoid Eucelatoria bryani. Entomologia Experimentalis et applicata. 71, 33-39.
Reznik, S. Y. and Vaghina, N. P. (2006). Temperature effects on induction of parasitization by females of Trichogramma principium (Hymenoptera, Trichogrammatidae). Entomol. Rev. 86, 133-138. doi:10.1134/S0013873806020023
Ringel,M. S., Rees, M. and Godfray, H. C. J. (1998). The evolution of diapause in a coupled host-parasitoid system. J. Theor. Biol. 194, 195-204. doi:10.1006/jtbi. 1998.0754
Rohmer, C., David, J. R., Moreteau, B. and Joly, D. (2004). Heat induced male sterility in Drosophila melanogaster: adaptive genetic variations among geographic populations and role of the Y chromosome. J. Exp. Biol. 207, 2735-2743. doi:10.1242/jeb.01087
Rosenzweig, M., Kang, K. J. and Garrity, P. A. (2008). Distinct TRP channels are required for warm and cool avoidance in Drosophila melanogaster. Proc. Natl. Acad. Sci. U. S. A. 105, 14668-14673. doi:10.1073/pnas.0805041105
Roux, O., Le Lann, C., Van Alphen, J. J. M. and Van Baaren, J. (2010). How does heat shock affect the life history traits of adults and progeny of the aphid parasitoid Aphidius avenae (Hymenoptera: Aphidiidae)? Bull. Entomol. Res. 100, 543-549. doi:10.1017/S0007485309990575
Salachan, P. V. and S rensen, J. G. (2017). Critical thermal limits affected differently by developmental and adult thermal fluctuations. J. Exp. Biol. 220, 4471-4478. doi:10.1242/jeb.165308
Salman, M. H. R., Bonsignore, C. P., El Alaoui El Fels, A., Giomi, F., Hodar, J. A., Laparie, M., Marini, L., Merel, C., Zalucki, M. P., Zamoum, M. and Battisti, A. (2019). Winter temperature predicts prolonged diapause in pine processionary moth species across their geographic range. PeerJ 7, e6530. doi:10.7717/peerj. 6530
Scheiner, S. M. (2013). The genetics of phenotypic plasticity. XII. Temporal and spatial heterogeneity. Ecol. Evol. 3, 4596-4609. doi:10.1002/ece3.792
Scheiner, S. M. (2014). The genetics of phenotypic plasticity. XIII. Interactions with developmental instability. Ecol. Evol. 4, 1347-1360. doi:10.1002/ece3.1039
Schou, M. F., Loeschcke, V. and Kristensen, T. N. (2015). Strong costs and benefits of winter acclimatization in Drosophila melanogaster. PLOS One 10, e0130307. doi:10.1371/journal.pone.0130307
Schro? ter, D., Cramer, W., Leemans, R., Prentice, I. C., Araujo, M. B., Arnell, N. W., Bondeau, A., Bugmann, H., Carter, T. R., Gracia, C. A., et al. (2005). Ecosystem service supply and vulnerability to global change in Europe. Science, 310, 1333-1337. doi:10.1126/science.1115233
Scott, M., Berrigan, D. and Hoffmann, A. A. (1997). Costs and benefits of acclimation to elevated temperature in Trichogramma carverae. Entomol. Exp. Appl. 85, 211-219. doi:10.1046/j.1570-7458.1997.00251.x
Seger, J. and Brockman, H. J. (1987). What is bet-hedging? In Oxford Surveys in Evolutionary Biology (ed. P. H. Harvey and L. Partridge), pp. 182-211. Oxford University Press.
Senior, V. L., Evans, L. C., Leather, S. R., Oliver, T. H. and Evans, K. L. (2020). Phenological responses in a sycamore-aphid-parasitoid system and consequences for aphid population dynamics: a 20 year case study. Glob. Change Biol. 26, 2814-2828. doi:10.1111/gcb.15015
Sgro, C. M., Terblanche, J. S. and Hoffmann, A. A. (2016). What can plasticity contribute to insect responses to climate change? Annu. Rev. Entomol. 61, 433-451. doi:10.1146/annurev-ento-010715-023859
Simons, A. M. (2011). Modes of response to environmental change and the elusive empirical evidence for bet hedging. Proc. R. Soc. B Biol. Sci. 278, 1601-1609. doi:10.1098/rspb.2011.0176
Smith, R. H. and Shaw, M. R. (1980). Haplodiploid sex ratios and the mutation rate. Nature 287, 728-729. doi:10.1038/287728a0
S rensen, J. G., Kristensen, T. N. and Loeschcke, V. (2003). The evolutionary and ecological role of heat shock proteins. Ecol. Lett. 6, 1025-1037. doi:10.1046/j. 1461-0248.2003.00528.x
S rensen, J. G., Kristensen, T. N., Loeschcke, V. and Schou, M. F. (2015). No trade-off between high and low temperature tolerance in a winter acclimatized Danish Drosophila subobscura population. J. Insect Physiol. 77, 9-14. doi:10. 1016/j.jinsphys.2015.03.014
S rensen, J. G., Schou, M. F., Kristensen, T. N. and Loeschcke, V. (2016). Thermal fluctuations affect the transcriptome through mechanisms independent of average temperature. Sci. Rep. 6, 1-11. doi:10.1038/srep30975
Starrfelt, J. and Kokko, H. (2012). Bet-hedging - a triple trade-off between means, variances and correlations. Biol. Rev. 87, 742-755. doi:10.1111/j.1469-185X. 2012.00225.x Stearns, S. C. (1989). Trade-offs in life-history evolution. Funct. Ecol. 3, 259-268. doi:10.2307/2389364
Tauber, M. J., Tauber, C. A. and Masaki, S. (1986). Seasonal Adaptations of Insects. Oxford University Press. Thomson, L. J., Robinson, M. and Hoffmann, A. A. (2001). Field and laboratory evidence for acclimation without costs in an egg parasitoid. Funct. Ecol. 15, 217-221. doi:10.1046/j.1365-2435.2001.00516.x
Torres, J. B., Musolin, D. L. and Zanuncio, J. C. (2002). Thermal requirements and parasitism capacity of Trissolcus brochymenae (Ashmead) (Hymenoptera: Scelionidae) under constant and fluctuating temperatures, and assessment of development in field conditions. Biocontrol Sci. Technol. 12, 583-593. doi:10. 1080/0958315021000016243
Tougeron, K., Brodeur, J., van Baaren, J., Renault, D. and Le Lann, C. (2019). Sex makes them sleepy: host reproductive status induces diapause in a parasitoid population experiencing harsh winters. Peer Community Ecol. 1-22. doi:10.1101/ 371385
Tougeron, K., Brodeur, J., Le Lann, C. and van Baaren, J. (2020a). How climate change affects the seasonal ecology of insect parasitoids. Ecol. Entomol. 45, 167-181. doi:10.1111/een.12792
Tougeron, K., Damien, M., Le Lann, C., Brodeur, J. and van Baaren, J. (2018b). Rapid responses of winter aphid-parasitoid communities to climate warming. Front. Ecol. Evol. 6, 173. doi:10.3389/fevo.2018.00173
Tougeron, K., Devogel, M., van Baaren, J., Le Lann, C. and Hance, T. (2020b). Trans-generational effects on diapause and life-history-traits of an aphid parasitoid. J. Insect Physiol. 121, 104001. doi:10.1016/j.jinsphys.2019.104001
Tougeron, K., Hraoui, G., Le Lann, C., van Baaren, J. and Brodeur, J. (2018a). Intraspecific maternal competition induces summer diapause in insect parasitoids. Insect Sci. 25, 1080-1088. doi:10.1111/1744-7917.12491
Tougeron, K., Le Lann, C., Brodeur, J. and van Baaren, J. (2017). Are aphid parasitoids from mild winter climates losing their winter diapause? Oecologia 183, 619-629. doi:10.1007/s00442-016-3770-7
Tougeron, K., van Baaren, J., Burel, F. and Alford, L. (2016). Comparing thermal tolerance across contrasting landscapes: first steps towards understanding how landscape management could modify ectotherm thermal tolerance. Insect Conserv. Divers. 9, 171-180. doi:10.1111/icad.12153
Tsukada, M. (1999). Interpopulation variation of hibernal-aestival-diapause in the egg parasitoid wasp Anagrus takeyanus: adaptation to seasonal host-plant alternation of the tingid host, Stephanitis takeyai. Entomol. Exp. Appl. 92, 37-43. doi:10.1046/j.1570-7458.1999.00522.x
Tufto, J. (2015). Genetic evolution, plasticity, and bet-hedging as adaptive responses to temporally autocorrelated fluctuating selection: a quantitative genetic model. Evolution (N. Y) 69, 2034-2049. doi:10.1111/evo.12716
Uller, T., Nakagawa, S. and English, S. (2013). Weak evidence for anticipatory parental effects in plants and animals. J. Evol. Biol. 26, 2161-2170. doi:10.1111/ jeb.12212
van Baaren, J. and Candolin, U. (2018). Plasticity in a changing world: behavioural responses to human perturbations. Curr. Opin. Insect Sci. 27, 21-25. doi:10.1016/ j.cois.2018.02.003
Vasseur, D. A., DeLong, J. P., Gilbert, B., Greig, H. S., Harley, C. D. G., McCann, K. S., Savage, V., Tunney, T. D. and O'Connor, M. I. (2014). Increased temperature variation poses a greater risk to species than climate warming. Proc. R. Soc. B Biol. Sci. 281, 20132612. doi:10.1098/rspb.2013.2612
Wang, D. S., He, Y. R., Zhang,W., Nian, X. G., Lin, T. and Zhao, R. (2014). Effects of heat stress on the quality of Trichogrammatoidea bactrae Nagaraja (Hymenoptera: Trichogrammatidae). Bull. Entomol. Res. 104, 543-551. doi:10. 1017/S0007485314000303
Xue, Q., Majeed, M. Z., Zhang, W. and Ma, C. (2019). Adaptation of Drosophila species to climate change - a literature review since 2003. J. Integr. Agric. 18, 805-814. doi:10.1016/S2095-3119(18)62042-8
Zwoinska, M. K., Rodrigues, L. R., Slate, J. and Snook, R. R. (2020). Phenotypic responses to and genetic architecture of sterility following exposure to sub-lethal temperature during development. Front. Genet. 11, 1-12. doi:10.3389/fgene. 2020.00573
