[en] This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY
Disciplines :
Zoology
Author, co-author :
Nieberding, Caroline ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement (Arlon Campus Environnement) > Zoogéographie ; Evolutionary Ecology and Genetics Group, Earth and Life Institute, UCLouvain, Louvain-la-Neuve, Belgium
Marcantonio, Matteo; Evolutionary Ecology and Genetics Group, Earth and Life Institute, UCLouvain, Louvain-la-Neuve, Belgium
Voda, Raluca; Evolutionary Ecology and Genetics Group, Earth and Life Institute, UCLouvain, Louvain-la-Neuve, Belgium
Enriquez, Thomas ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs ; Evolution and Ecophysiology Group, Earth and Life Institute, UCLouvain, Louvain-la-Neuve, Belgium
Visser, Bertanne ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs ; Evolution and Ecophysiology Group, Earth and Life Institute, UCLouvain, Louvain-la-Neuve, Belgium
Language :
English
Title :
The Evolutionary Relevance of Social Learning and Transmission in Non-Social Arthropods with a Focus on Oviposition-Related Behaviors
Whiten, A.; Caldwell, C.A.; Mesoudi, A. Cultural diffusion in humans and other animals. Curr. Opin. Psychol. 2016, 8, 15–21, doi:10.1016/j.copsyc.2015.09.002.
Fisher, J.; Hinde, R. Opening of milk bottles by birds. Br. Birds 1950, 42, 347–357, doi:10.1038/165435a0.
Heyes, C.M.; Street, G. Social learning in animals: Categories and mechanisms. Biol. Rev. 1994, 69, 207–231.
Morand‐Ferron, J. Why learn? The adaptive value of associative learning in wild populations. Curr. Opin. Behav. Sci. 2017, 16, 73–79, doi:10.1016/j.cobeha.2017.03.008.
Morand‐Ferron, J.; Cole, E.F.; Quinn, J.L. Studying the evolutionary ecology of cognition in the wild: a review of practical and conceptual challenges. Biol. Rev. 2016, 91, 367–389, doi:10.1111/brv.12174.
Baldwin, J. A new factor in evolution. Am. Nat. 1896, 30, 441–451.
Whiten, A. A second inheritance system: The extension of biology through culture. Interface Focus 2017, 7, 20160142, doi:10.1098/rsfs.2016.0142.
Whiten, A. Culture extends the scope of evolutionary biology in the great apes. Proc. Natl. Acad. Sci. USA 2017, 114, 7790–7797, doi:10.1073/pnas.1620733114.
Hoppitt, W.; Laland, K. Social Learning: An Introduction to Mechanisms, Methods, and Models; Princeton University Press: Prince-ton, NJ, USA, 2013;
Slater, P.J.B. The cultural transmission of bird song. Trends Ecol. Evol. 1986, 1, 94–97, doi:10.1016/0169‐5347(86)90032‐7.
Deecke, V.B.; Ford, J.K.B.; Spong, P. Dialect change in resident killer whales: Implications for vocal learning and cultural trans-mission. Anim. Behav. 2000, 60, 629–638, doi:10.1006/anbe.2000.1454.
Garland, E.C.; Goldizen, A.W.; Rekdahl, M.L.; Constantine, R.; Garrigue, C.; Hauser, N.D.; Poole, M.M.; Robbins, J.; Noad, M.J. Dynamic horizontal cultural transmission of humpback whale song at the ocean basin scale. Curr. Biol. 2011, 21, 687–691, doi:10.1016/j.cub.2011.03.019.
Cantor, M.; Whitehead, H. The interplay between social networks and culture: Theoretically and among whales and dolphins. Philos. Trans. R. Soc. B Biol. Sci. 2013, 368, 20120340, doi:10.1098/rstb.2012.0340.
Lamon, N.; Neumann, C.; Gruber, T.; Zuberbühler, K. Kin‐based cultural transmission of tool use in wild chimpanzees. Sci. Adv. 2017, 3, 1–10, doi:10.1126/sciadv.1602750.
Alem, S.; Perry, C.J.; Zhu, X.; Loukola, O.J.; Ingraham, T.; Søvik, E.; Chittka, L. Associative Mechanisms Allow for Social Learning and Cultural Transmission of String Pulling in an Insect. PLoS Biol. 2016, 14, e1002564, doi:10.1371/journal.pbio.1002564.
Nieberding, C.M.; van Alphen, J.J. Culture in bumblebees. Peer Community Evol. Biol. 2017, 2–4, doi:10.24072/pci.evolbiol.100001.
Grüter, C.; Leadbeater, E. Insights from insects about adaptive social information use. Trends Ecol. Evol. 2014, 29, 177–184, doi:10.1016/j.tree.2014.01.004.
Avarguès‐Weber, A.; Lihoreau, M.; Isabel, G.; Giurfa, M. Information transfer beyond the waggle dance: Observational learning in bees and flies. Front. Ecol. Evol. 2015, 3, 1–7, doi:10.3389/fevo.2015.00024.
Worden, B.D.; Papaj, D.R. Flower choice copying in bumblebees. Biol. Lett. 2005, 1, 504–507, doi:10.1098/rsbl.2005.0368.
Jones, P.L.; Agrawal, A.A. Learning in Insect Pollinators and Herbivores. Annu. Rev. Entomol. 2017, 62, 53–71, doi:10.1146/an-nurev‐ento‐031616‐034903.
Kacsoh, B.Z.; Bozler, J.; Ramaswami, M.; Bosco, G. Social communication of predator‐induced changes in Drosophila behavior and germline physiology. Elife 2015, 4, 1–36, doi:10.7554/eLife.07423.
Kacsoh, B.; Bozler, J.; Bosco, G. Drosophila species learn dialects through communal living. PLoS Genet. 2018, 14, e1007430, doi:10.1101/206920.
Danchin, É.; Nobel, S.; Pocheville, A.; Dagaeff, A.‐C.; Demay, L.; Alphand, M.; Ranty‐Roby, S.; van Renssen, L.; Monier, M.; Gazagne, E.; et al. Cultural flies: Conformist social learning in fruitflies predicts long‐lasting mate‐choice traditions. Science 2019, 366, 1–7, doi:10.1126/science.aaw8012.
Durisko, Z.; Dukas, R. Attraction to and learning from social cues in fruitfly larvae. Proc. R. Soc. B Biol. Sci. 2013, 280, 1–7, doi:10.1098/rspb.2013.1398.
Battesti, M.; Moreno, C.; Joly, D.; Mery, F. Spread of social information and dynamics of social transmission within Drosophila groups. Curr. Biol. 2012, 22, 309–313, doi:10.1016/j.cub.2011.12.050.
Coolen, I.; Dangles, O.; Casas, J. Social learning in noncolonial insects? Curr. Biol. 2005, 15, 1931–1935, doi:10.1016/j.cub.2005.09.015.
McDowell, J.M. Genomes of obligate plant pathogens reveal adaptations for obligate parasitism. Proc. Natl. Acad. Sci. USA 2011, 108, 8921–8922, doi:10.1073/pnas.1105802108.
Mery, F.; Varela, S.A.M.; Danchin, É.; Blanchet, S.; Parejo, D.; Coolen, I.; Wagner, R.H. Public versus personal information for mate copying in an invertebrate. Curr. Biol. 2009, 19, 730–734, doi:10.1016/j.cub.2009.02.064.
Belkina, E.G.; Shiglik, A.; Sopilko, N.G.; Lysenkov, S.N.; Markov, A.V. Mate choice copying in Drosophila is probably less robust than previously suggested. Anim. Behav. 2021, 176, 175–183.
Dion, E.; Monteiro, A.; Nieberding, C.M. The role of learning on insect and spider sexual behaviors, sexual trait evolution, and speciation. Front. Ecol. Evol. 2019, 6, 225, doi:10.3389/fevo.2018.00225.
Dukas, R. Evolutionary biology of insect learning. Annu. Rev. Entomol. 2008, 53, 145–160, doi:10.1146/an-nurev.ento.53.103106.093343.
Wright, G.A.; Schiestl, F.P. The evolution of floral scent: The influence of olfactory learning by insect pollinators on the honest signalling of floral rewards. Funct. Ecol. 2009, 23, 841–851, doi:10.1111/j.1365‐2435.2009.01627.x.
Webster, S.J.; Fiorito, G. Socially guided behaviour in non‐insect invertebrates. Anim. Cogn. 2001, 4, 69–79, doi:10.1007/s100710100108.
Hoedjes, K.M.; Kruidhof, H.M.; Huigens, M.E.; Dicke, M.; Vet, L.E.M.; Smid, H.M. Natural variation in learning rate and memory dynamics in parasitoid wasps: Opportunities for converging ecology and neuroscience. Proc. R. Soc. B Biol. Sci. 2011, 278, 889–897, doi:10.1098/rspb.2010.2199.
Traynier, R.M.M. Associative learning in the ovipositional behaviour of the cabbage butterfly, Pieris rapae. Physiol. Entomol. 1984, 9, 465–472, doi:10.1111/j.1365‐3032.1984.tb00789.x.
Papaj, D.R. Interpopulation differences in host preference and the evolution of learning in the butterfly, Battus philenor. Evolution 1986, 40, 518–530, doi:10.1111/j.1558‐5646.1986.tb00504.x.
Traynier, R.M.M. Visual learning in assays of sinigrin solution as an oviposition releaser for the cabbage butterfly, Pieris rapae. Entomol. Exp. Appl. 1986, 40, 25–33, doi:10.1111/j.1570‐7458.1986.tb02151.x.
Visser, M.E.; van Alphen, J.J.; Hemerik, L. Adaptive superparasitism and patch time allocation in solitary parasitoids: An ESS model. J. Anim. Ecol. 1992, 61, 93–101.
Vet, L.E.M.; De Jong, A.G.; Franchi, E.; Papaj, D.R. The effect of complete versus incomplete information on odour discrimina-tion in a parasitic wasp. Anim. Behav. 1998, 55, 1271–1279, doi:10.1006/anbe.1997.0686.
Mery, F.; Kawecki, T.J. Experimental evolution of learning ability in fruit flies. Proc. Natl. Acad. Sci. USA 2002, 99, 14274–14279, doi:10.1073/pnas.222371199.
Liu, S.S.; Li, Y.H.; Liu, Y.Q.; Zalucki, M.P. Experience‐induced preference for oviposition repellents derived from a non‐host plant by a specialist herbivore. Ecol. Lett. 2005, 8, 722–729, doi:10.1111/j.1461‐0248.2005.00776.x.
Braem, S.; Turlure, C.; Nieberding, C.; van Dyck, H. Oviposition site selection and learning in a butterfly under niche expansion: An experimental test. Anim. Behav. 2021, in press.
Kawecki, T.J. Evolutionary ecology of learning: Insights from fruit flies. Popul. Ecol. 2010, 52, 15–25, doi:10.1007/s10144‐009‐ 0174‐0.
Danchin, É.; Wagner, R.H. Inclusive heritability: Combining genetic and non‐genetic information to study animal behavior and culture. Oikos 2010, 119, 210–218, doi:10.1111/j.1600‐0706.2009.17640.x.
Mesoudi, A.; Chang, L.; Dall, S.R.X.; Thornton, A. The evolution of individual and cultural variation in social learning. Trends Ecol. Evol. 2016, 31, 215–225, doi:10.1016/j.tree.2015.12.012.
Danchin, E.; Pocheville, A.; Rey, O.; Pujol, B.; Blanchet, S. Epigenetically facilitated mutational assimilation: epigenetics as a hub within the inclusive evolutionary synthesis. Biol. Rev. 2019, 94, 259–282, doi:10.1111/brv.12453.
Reaume, C.J.; Sokolowski, M.B. Conservation of gene function in behaviour. Philos. Trans. R. Soc. B Biol. Sci. 2011, 366, 2100– 2110, doi:10.1098/rstb.2011.0028.
Bengston, S.E.; Dahan, R.A.; Donaldson, Z.; Phelps, S.M.; Van Oers, K.; Sih, A.; Bell, A.M. Genomic tools for behavioural ecologists to understand repeatable individual differences in behaviour. Nat. Ecol. Evol. 2018, 2, 944–955, doi:10.1038/s41559‐017‐ 0411‐4.
Henriksen, R.; Höglund, A.; Fogelholm, J.; Abbey‐Lee, R.; Johnsson, M.; Dingemanse, N.J.; Wright, D. Intra‐individual behavioural variability: A trait under genetic control. Int. J. Mol. Sci. 2020, 21, 1–21, doi:10.3390/ijms21218069.
Bubac, C.M.; Miller, J.M.; Coltman, D.W. The genetic basis of animal behavioural diversity in natural populations. Mol. Ecol. 2020, 29, 1957–1971, doi:10.1111/mec.15461.
Williams‐Simon, P.A.; Posey, C.; Mitchell, S.; Ng’oma, E.; Mrkvicka, J.A.; Zars, T.; King, E.G. Multiple genetic loci affect place learning and memory performance in Drosophila melanogaster. Genes Brain Behav. 2019, 18, 1–16, doi:10.1111/gbb.12581.
Mery, F. Natural variation in learning and memory. Curr. Opin. Neurobiol. 2013, 23, 52–56, doi:10.1016/j.conb.2012.09.001.
Hughes, E.; Shymansky, T.; Swinton, E.; Lukowiak, K.S.; Swinton, C.; Sunada, H.; Protheroe, A.; Phillips, I.; Lukowiak, K. Strain-specific differences of the effects of stress on memory in Lymnaea. J. Exp. Biol. 2017, 220, 891–899, doi:10.1242/jeb.149161.
Giunti, G.; Canale, A.; Messing, R.H.; Donati, E.; Stefanini, C.; Michaud, J.P.; Benelli, G. Parasitoid learning: Current knowledge and implications for biological control. Biol. Control 2015, 90, 208–219, doi:10.1016/j.biocontrol.2015.06.007.
Liefting, M.; Verwoerd, L.; Dekker, M.L.; Hoedjes, K.M.; Ellers, J. Strain differences rather than species differences contribute to variation in associative learning ability in Nasonia. Anim. Behav. 2020, 168, 25–31, doi:10.1016/j.anbehav.2020.07.026.
Osborne, K.A.; Robichon, A.; Burgess, E.; Butland, S.; Shaw, R.A.; Coulthard, A.; Pereira, H.S.; Greenspan, R.J.; Sokolowski, M.B. Natural behavior polymorphism due to a cGMP‐dependent protein kinase of Drosophila. Science 1997, 277, 834–836, doi:10.1126/science.277.5327.834.
Wahlberg, N.; Wheat, C.W.; Peña, C. Timing and patterns in the taxonomic diversification of Lepidoptera (butterflies and moths). PLoS One 2013, 8, e80875.
Wheat, C.W. Dispersal genetics: emerging insights from fruitflies, butterflies, and beyond. In Dispersal Ecology and Evolution; Clobert, J., Baguette, M., Benton, T., Bullock, J., Eds.; 2012; p. 498. Oxford University Press, Oxford.
Fitzpatrick, M.J.; Sokolowski, M.B. In search of food: Exploring the evolutionary link between cGMP‐dependent protein kinase (PKG) and behaviour. Integr. Comp. Biol. 2004, 44, 28–36, doi:10.1093/icb/44.1.28.
Gapp, K.; Jawaid, A.; Sarkies, P.; Bohacek, J.; Pelczar, P.; Prados, J.; Farinelli, L.; Miska, E.; Mansuy, I.M. Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat. Neurosci. 2014, 17, 667–669, doi:10.1038/nn.3695.
Charlesworth, A.G.; Seroussi, U.; Claycomb, J.M. Next‐Gen Learning: The C. elegans Approach. Cell 2019, 177, 1674–1676, doi:10.1016/j.cell.2019.05.039.
Posner, R.; Toker, I.A.; Antonova, O.; Star, E.; Anava, S.; Azmon, E.; Hendricks, M.; Bracha, S.; Gingold, H.; Rechavi, O. Neuronal small RNAs control behavior transgenerationally. Cell 2019, 177, 1814–1826.e15, doi:10.1016/j.cell.2019.04.029.
Rösvik, A.; Lhomme, P.; Khallaf, M.A.; Anderson, P. Plant‐induced transgenerational plasticity affecting performance but not preference in a polyphagous moth. Front. Ecol. Evol. 2020, 8, 1–9, doi:10.3389/fevo.2020.00254.
Barrett, L.P.; Stanton, L.A.; Benson‐Amram, S. The cognition of ‘nuisance’ species. Anim. Behav. 2019, 147, 167–177, doi:10.1016/j.anbehav.2018.05.005.
Rausher, M.D. Search image for leaf shape in a butterfly. Science 1978, 200, 1071–1073.
Williams, K.S.; Gilbert, L.E. Insects as selective agents on plant vegetative morphology: Egg mimicry reduces egg laying by butterflies. Science 1981, 212, 467–469, doi:10.1126/science.212.4493.467.
Bar‐On, Y.M.; Phillips, R.; Milo, R. The biomass distribution on Earth. Proc. Natl. Acad. Sci. USA 2018, 115, 6506, doi:10.1073/pnas.1711842115.
Mora, C.; Tittensor, D.P.; Adl, S.; Simpson, A.G.B.; Worm, B. How many species are there on earth and in the ocean? PLoS Biol. 2011, 9, e1001127, doi:10.1371/journal.pbio.1001127.
Ellner, S.; Hairston, N.G., Jr. Role of overlapping generations in maintaining genetic variation in a fluctuating environment. Am. Nat. 1994, 143, 403–417, doi:10.1086/285610.
Choe, J.; Crespi, B. The Evolution of Social Behavior in Insects and Arachnids; Cambridge University Press: Cambridge, UK, 1997.
Costa, J. The Other Insect Societies; Harvard University Press: Cambridge, MA, USA, 2006.
Costa, J. Social evolution in “other” insects and arachnids. In Encyclopedia of Animal Behavior; Breed, M., Moore, J., Eds.; Aca-demic Press: Cambridge, MA, USA, 2016.
Costa, J.T. The other insect societies: overview and new directions. Curr. Opin. Insect Sci. 2018, 28, 40–49, doi:10.1016/j.cois.2018.04.008.
Aluja, M.; Díaz‐Fleischer, F. Foraging behavior of Anastrepha ludens, A. obliqua, and A. serpentina in response to feces extracts containing host marking pheromone. J. Chem. Ecol. 2006, 32, 367–389, doi:10.1007/s10886‐005‐9007‐6.
Decker, A.; D’elia, B.; Kuhl, A.; Rosen, S.; Disney, A.; Dial, C.; Linietsky, M.; Taylor‐Lilquist, J.; Taylor‐Lilquist, B.; Kim, E.; et al. Acoustic stimulus influences ovipositioning in Drosophila melanogaster. Bull. Insectol. 2020, 73, 103–109.
Corbet, S.A. Mandibular gland secretion of larvae of the flour moth, Anagasta kuehniella, contains an epideictic pheromone and elicits oviposition movements in a hymenopteran parasite. Nature 1971, 232, 481–484, doi:10.1038/232481b0.
Otake, R.; Dobata, S. Copy if dissatisfied, innovate if not: contrasting egg‐laying decision making in an insect. Anim. Cogn. 2018, 21, 805–812, doi:10.1007/s10071‐018‐1212‐0.
Malek, H.L.; Long, T.A.F. On the use of private versus social information in oviposition site choice decisions by Drosophila melanogaster females. Behav. Ecol. 2020, 31, 739–749, doi:10.1093/beheco/araa021.
Battesti, M.; Moreno, C.; Joly, D.; Mery, F. Biased social transmission in Drosophila oviposition choice. Behav. Ecol. Sociobiol. 2015, 69, 83–87, doi:10.1007/s00265‐014‐1820‐x.
Battesti, M.; Pasquaretta, C.; Moreno, C.; Teseo, S.; Joly, D.; Klensch, E.; Petit, O.; Sueur, C.; Mery, F. Ecology of information: Social transmission dynamics within groups of non‐social insects. Proc. R. Soc. B Biol. Sci. 2015, 282, 20142480, doi:10.1098/rspb.2014.2480.
Elsensohn, J.E.; Aly, M.F.K.; Schal, C.; Burrack, H.J. Social signals mediate oviposition site selection in Drosophila suzukii. Sci. Rep. 2021, 11, 1–10, doi:10.1038/s41598‐021‐83354‐2.
Stelinski, L.L.; Rodriguez‐Saona, C.; Meyer, W.L. Recognition of foreign oviposition‐marking pheromone in a multi‐trophic context. Naturwissenschaften 2009, 96, 585–592, doi:10.1007/s00114‐009‐0507‐z.
Pasqualone, A.A.; Davis, J.M. The use of conspecific phenotypic states as information during reproductive decisions. Anim. Behav. 2011, 82, 281–284, doi:10.1016/j.anbehav.2011.05.002.
Yadav, P.; Desireddy, S.; Kasinathan, S.; Bessière, J.M.; Borges, R.M. History matters: Oviposition resource acceptance in an exploiter of a nursery pollination mutualism. J. Chem. Ecol. 2018, 44, 18–28, doi:10.1007/s10886‐017‐0914‐0.
Godfray, H.C.J. Parasitoids: Behavioural and Evolutionary Ecology; Princeton University Press: West Sussex, NJ, USA, 1994.
Loukola, O.J.; Gatto, E.; Híjar‐Islas, A.C.; Chittka, L. Selective interspecific information use in the nest choice of solitary bees. Anim. Biol. 2020, 70, 215–225, doi:10.1163/15707563‐20191233.
Huigens, M.E.; Pashalidou, F.G.; Qian, M.H.; Bukovinszky, T.; Smid, H.M.; Van Loon, J.J.A.; Dicke, M.; Fatouros, N.E. Hitch-hiking parasitic wasp learns to exploit butterfly antiaphrodisiac. Proc. Natl. Acad. Sci. USA 2009, 106, 820–825, doi:10.1073/pnas.0812277106.
Sarin, S.; Dukas, R. Social learning about egg‐laying substrates in fruitflies. Proc. R. Soc. B Biol. Sci. 2009, 276, 4323–4328, doi:10.1098/rspb.2009.1294.
Couty, A.; Kaiser, L.; Huet, D.; Pham‐Delegue, M.H. The attractiveness of different odour sources from the fruit‐host complex on Leptopilina boulardi, a larval parasitoid of frugivorous Drosophila spp. Physiol. Entomol. 1999, 24, 76–82, doi:10.1046/j.1365‐ 3032.1999.00116.x.
Bodino, N.; Ferracini, C.; Tavella, L. Is host selection influenced by natal and adult experience in the parasitoid Necremnus tutae (Hymenoptera: Eulophidae)? Anim. Behav. 2016, 112, 221–228, doi:10.1016/j.anbehav.2015.12.011.
Ghimire, M.N.; Phillips, T.W. Effects of prior experience on host selection and host utilization by two populations of Anisopter-omalus calandrae (Hymenoptera: Pteromalidae). Environ. Entomol. 2008, 37, 1300–1306, doi:10.1603/0046‐225X(2008)37[1300:EO‐ PEOH]2.0.CO;2.
Stephan, J.G.; Stenberg, J.A.; Björkman, C. How far away is the next basket of eggs? Spatial memory and perceived cues shape aggregation patterns in a leaf beetle. Ecology 2015, 96, 908–914, doi:10.1890/14‐1143.1.
Murase, A.; Fujita, K.; Yano, S. Behavioural flexibility in spider mites: Oviposition site shifts based on past and present stimuli from conspecifics and predators. R. Soc. Open Sci. 2017, 4, 170328, doi:10.1098/rsos.170328.
Kujtan, L.; Dukas, R. Learning magnifies individual variation in heterospecific mating propensity. Anim. Behav. 2009, 78, 549– 554, doi:10.1016/j.anbehav.2009.05.026.
Mair, M.M.; Seifert, N.; Ruther, J. Previous interspecific courtship impairs female receptivity to conspecifics in the parasitoid wasp Nasonia longicornis but not in N. vitripennis. Insects 2018, 9, 112, doi:10.3390/insects9030112.
Hostachy, C.; Couzi, P.; Portemer, G.; Hanafi‐Portier, M.; Murmu, M.; Deisig, N.; Dacher, M. Exposure to conspecific and het-erospecific sex‐pheromones modulates gustatory habituation in the moth Agrotis ipsilon. Front. Physiol. 2019, 10, 1–8, doi:10.3389/fphys.2019.01518.
Romano, D.; Benelli, G.; Stefanini, C. Opposite valence social information provided by bio‐robotic demonstrators shapes selection processes in the green bottle fly. J. R. Soc. Interface 2021, 18, 20210056.
Verzijden, M.N.; ten Cate, C.; Servedio, M.R.; Kozak, G.M.; Boughman, J.W.; Svensson, E. The impact of learning on sexual selection and speciation. Trends Ecol. Evol. 2012, 27, 511–519, doi:doi:10.1016/j.tree.2012.05.007.
Vosteen, I.; van den Meiracker, N.; Poelman, E.H. Getting confused: learning reduces parasitoid foraging efficiency in some environments with non‐host‐infested plants. Oecologia 2019, 189, 919–930, doi:10.1007/s00442‐019‐04384‐2.
Magrath, R.D.; Haff, T.M.; Fallow, P.M.; Radford, A.N. Eavesdropping on heterospecific alarm calls: From mechanisms to con-sequences. Biol. Rev. 2015, 90, 560–586, doi:10.1111/brv.12122.
Muramatsu, D. Sand‐bubbler crabs distinguish fiddler crab signals to predict intruders. Behav. Ecol. Sociobiol. 2021, 75, 1–11, doi:10.1007/s00265‐021‐03066‐5.
Rieucau, G.; Giraldeau, L.A. Exploring the costs and benefits of social information use: An appraisal of current experimental evidence. Philos. Trans. R. Soc. B Biol. Sci. 2011, 366, 949–957, doi:10.1098/rstb.2010.0325.
Nieberding; Van Dyck, H.; Chittka, L. Adaptive learning in non‐social insects: from theory to field work, and back. Curr. Opin. Insect Sci. 2018, 27, 75–81, doi:https://doi.org/10.1016/j.cois.2018.03.008.
Costa, T.M.; Hebets, E.A.; Melo, D.; Willemart, R.H. Costly learning: Preference for familiar food persists despite negative impact on survival. Biol. Lett. 2016, 12, 20160256, doi:10.1098/rsbl.2016.0256.
Botero, C.A.; Weissing, F.J.; Wright, J.; Rubenstein, D.R. Evolutionary tipping points in the capacity to adapt to environmental change. Proc. Natl. Acad. Sci. USA 2015, 112, 184–189, doi:10.1073/pnas.1408589111.
Dechaume‐Moncharmont, F.X.; Dornhaus, A.; Houston, A.I.; McNamara, J.M.; Collins, E.J.; Franks, N.R. The hidden cost of information in collective foraging. Proc. R. Soc. B Biol. Sci. 2005, 272, 1689–1695, doi:10.1098/rspb.2005.3137.
Greggor, A.L.; Trimmer, P.C.; Barrett, B.J.; Sih, A. Challenges of Learning to Escape Evolutionary Traps. Front. Ecol. Evol. 2019, 7, 408, doi:10.3389/fevo.2019.00408.
Fleury, F.; Gibert, P.; Ris, N.; Allemand, R. Ecology and life history evolution of frugivorous Drosophila parasitoids. Adv. Para-sitol. 2009, 70, 3–44, doi:10.1016/S0065‐308X(09)70001‐6.
Lefèvre, T.; De Roode, J.C.; Kacsoh, B.Z.; Schlenke, T.A. Defence strategies against a parasitoid wasp in Drosophila: Fight or flight? Biol. Lett. 2012, 8, 230–233, doi:10.1098/rsbl.2011.0725.
van Lenteren, J.C.; Bakker, K. Behavioural aspects of the functional responses of a parasite (Pseudocoila bochei) to its host (Dro-sophila melanogaster). Netherlands J. Zool. 1978, 28, 213–233.
Vet, L.E.; Papaj, D. Effects of experience on parasitoid movement in odour plumes. Physiol. Entomol. 1992, 17, 90–96, doi:10.1111/j.1365‐3032.1992.tb00994.x.
Wertheim, B.; Vet, L.E.M.; Dicke, M. Increased risk of parasitism as ecological costs of using aggregation pheromones: Labora-tory and field study of Drosophila‐Leptopilina interaction. Oikos 2003, 100, 269–282.
