Evolutionary divergence of developmental plasticity and learning of mating tactics in Trinidadian guppies.
G × E interaction
alternative mating tactic
behavioural plasticity
brain morphology
guppy
predation
social learning
Journal
The Journal of animal ecology
ISSN: 1365-2656
Titre abrégé: J Anim Ecol
Pays: England
ID NLM: 0376574
Informations de publication
Date de publication:
29 Dec 2023
29 Dec 2023
Historique:
received:
30
08
2023
accepted:
30
11
2023
medline:
29
12
2023
pubmed:
29
12
2023
entrez:
29
12
2023
Statut:
aheadofprint
Résumé
Behavioural plasticity is a major driver in the early stages of adaptation, but its effects in mediating evolution remain elusive because behavioural plasticity itself can evolve. In this study, we investigated how male Trinidadian guppies (Poecilia reticulata) adapted to different predation regimes diverged in behavioural plasticity of their mating tactic. We reared F2 juveniles of high- or low-predation population origins with different combinations of social and predator cues and assayed their mating behaviour upon sexual maturity. High-predation males learned their mating tactic from conspecific adults as juveniles, while low-predation males did not. High-predation males increased courtship when exposed to chemical predator cues during development; low-predation males decreased courtship in response to immediate chemical predator cues, but only when they were not exposed to such cues during development. Behavioural changes induced by predator cues were associated with developmental plasticity in brain morphology, but changes acquired through social learning were not. We thus show that guppy populations diverged in their response to social and ecological cues during development, and correlational evidence suggests that different cues can shape the same behaviour via different neural mechanisms. Our study demonstrates that behavioural plasticity, both environmentally induced and socially learnt, evolves rapidly and shapes adaptation when organisms colonize ecologically divergent habitats. 行為可塑性是驅動生態適應早期階段的一個重要因素,但由於行為可塑性本身也能在演化中改變,其確切效應仍難以定位。 在這項研究中,我們探討千里達的孔雀魚 (Poecilia reticulata) 雄魚繁殖策略(求偶或是直接試圖交配)的行為可塑性在不同掠食壓力下的趨異適應。我們利用源於高或低掠食壓力族群的F2幼魚,將其養殖於有不同掠食者訊號或同種個體的社會訊息的環境,並在性成熟時測量其交配策略。 高掠食壓力族群的雄魚在幼魚時期學習接觸的同種成魚的繁殖策略,而低掠食壓力族群的雄魚則沒有表現這種學習行為。幼魚時期接觸掠食者化學訊號的高掠食壓力族群雄魚在性成熟時表現較多的求偶行為;低掠食壓力族群雄魚,若在發育時期沒有接觸過掠食者化學訊號,他們在有掠食者化學訊號的環境中則會降低求偶行為。 掠食者化學訊號引起的行為變化與腦形態的發育可塑性相關,而通過學習同種成魚交配策略的變化則不相關。 因此,我們展示了孔雀魚族群對社會及生態訊號反應的繁殖行為可塑性的趨異適應。研究中腦發育與行為發育的相關性的證據亦顯示,由不同的訊號激發的行為可塑性可能為不同的神經機制所操控。 我們的研究顯示,無論是環境誘發還是社會學習造成的行為可塑性,皆能迅速演化並影響在生物對不同生態環境的適應過程。. La plasticidad conductual es un factor importante en las primeras fases de adaptación, pero se conocen poco sus efectos sobre la evolución porque la plasticidad conductual en sí puede evolucionar. En este estudio, investigamos cómo los machos del guppy de Trinidad (Poecilia reticulata) adaptados a regímenes de depredación diferentes, han divergido en la plasticidad de su táctica de apareamiento. Criamos juveniles provenientes de poblaciones de alta y baja depredación hasta segunda generación (F2) bajo diferentes combinaciones de señales sociales y de depredación, y evaluamos su comportamiento de apareamiento al llegar a la madurez sexual. Los machos de alta depredación aprendieron su táctica de apareamiento de sus conespecíficos adultos, mientras que los machos de baja depredación no. Los machos de alta depredación aumentaron su cortejo al ser expuestos a señales de depredadores durante su desarrollo; mientras que los machos de baja depredación redujeron su cortejo en respuesta a señales inmediatas de depredadores, pero tan solo cuando no fueron expuestos a tales señales durante el desarrollo. Los cambios conductuales observados inducidos por las señales de depredación están asociados con una plasticidad en el desarrollo de la morfología cerebral, pero los cambios adquiridos por aprendizaje social no. En conclusión, demostramos que las poblaciones de guppy han divergido en su respuesta a señales sociales y ecológicas durante su desarrollo, y mostramos evidencia correlativa que sugiere que diferentes tipos de señales pueden influenciar el mismo comportamiento via mecanismos neuronales diferentes. Nuestro estudio muestra que la plasticidad conductual, tanto inducida por el medio ambiente combo aprendida socialmente, evoluciona rápidamente e influencia la adaptación durante la colonización de hábitats ecológicamente divergentes.
Autres résumés
Type: Publisher
(kor)
行為可塑性是驅動生態適應早期階段的一個重要因素,但由於行為可塑性本身也能在演化中改變,其確切效應仍難以定位。 在這項研究中,我們探討千里達的孔雀魚 (Poecilia reticulata) 雄魚繁殖策略(求偶或是直接試圖交配)的行為可塑性在不同掠食壓力下的趨異適應。我們利用源於高或低掠食壓力族群的F2幼魚,將其養殖於有不同掠食者訊號或同種個體的社會訊息的環境,並在性成熟時測量其交配策略。 高掠食壓力族群的雄魚在幼魚時期學習接觸的同種成魚的繁殖策略,而低掠食壓力族群的雄魚則沒有表現這種學習行為。幼魚時期接觸掠食者化學訊號的高掠食壓力族群雄魚在性成熟時表現較多的求偶行為;低掠食壓力族群雄魚,若在發育時期沒有接觸過掠食者化學訊號,他們在有掠食者化學訊號的環境中則會降低求偶行為。 掠食者化學訊號引起的行為變化與腦形態的發育可塑性相關,而通過學習同種成魚交配策略的變化則不相關。 因此,我們展示了孔雀魚族群對社會及生態訊號反應的繁殖行為可塑性的趨異適應。研究中腦發育與行為發育的相關性的證據亦顯示,由不同的訊號激發的行為可塑性可能為不同的神經機制所操控。 我們的研究顯示,無論是環境誘發還是社會學習造成的行為可塑性,皆能迅速演化並影響在生物對不同生態環境的適應過程。.
Type: Publisher
(spa)
La plasticidad conductual es un factor importante en las primeras fases de adaptación, pero se conocen poco sus efectos sobre la evolución porque la plasticidad conductual en sí puede evolucionar. En este estudio, investigamos cómo los machos del guppy de Trinidad (Poecilia reticulata) adaptados a regímenes de depredación diferentes, han divergido en la plasticidad de su táctica de apareamiento. Criamos juveniles provenientes de poblaciones de alta y baja depredación hasta segunda generación (F2) bajo diferentes combinaciones de señales sociales y de depredación, y evaluamos su comportamiento de apareamiento al llegar a la madurez sexual. Los machos de alta depredación aprendieron su táctica de apareamiento de sus conespecíficos adultos, mientras que los machos de baja depredación no. Los machos de alta depredación aumentaron su cortejo al ser expuestos a señales de depredadores durante su desarrollo; mientras que los machos de baja depredación redujeron su cortejo en respuesta a señales inmediatas de depredadores, pero tan solo cuando no fueron expuestos a tales señales durante el desarrollo. Los cambios conductuales observados inducidos por las señales de depredación están asociados con una plasticidad en el desarrollo de la morfología cerebral, pero los cambios adquiridos por aprendizaje social no. En conclusión, demostramos que las poblaciones de guppy han divergido en su respuesta a señales sociales y ecológicas durante su desarrollo, y mostramos evidencia correlativa que sugiere que diferentes tipos de señales pueden influenciar el mismo comportamiento via mecanismos neuronales diferentes. Nuestro estudio muestra que la plasticidad conductual, tanto inducida por el medio ambiente combo aprendida socialmente, evoluciona rápidamente e influencia la adaptación durante la colonización de hábitats ecológicamente divergentes.
Identifiants
pubmed: 38156548
doi: 10.1111/1365-2656.14043
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : National Science Foundation
ID : DGE-2139839
Organisme : National Science Foundation
ID : IOS-1755071
Organisme : Cornell University
Organisme : Washington University in St. Louis
Organisme : University of South Florida
Informations de copyright
© 2023 The Authors. Journal of Animal Ecology © 2023 British Ecological Society.
Références
Abràmoff, M. D., Magalhães, P. J., & Ram, S. J. (2004). Image processing with imageJ. Biophotonics International, 11(7), 36-41. https://doi.org/10.1201/9781420005615.ax4
Álvarez, D., & Bell, A. M. (2007). Sticklebacks from streams are more bold than sticklebacks from ponds. Behavioural Processes, 76(3), 215-217. https://doi.org/10.1016/j.beproc.2007.05.004
Amo, L., López, P., & Martín, J. (2004). Wall lizards combine chemical and visual cues of ambush snake predators to avoid overestimating risk inside refuges. Animal Behaviour, 67(4), 647-653. https://doi.org/10.1016/j.anbehav.2003.08.005
Axelrod, C. J., Gordon, S. P., & Carlson, B. A. (2023). Integrating neuroplasticity and evolution. Current Biology, 33(8), R288-R293. https://doi.org/10.1016/j.cub.2023.03.002
Axelrod, C. J., Robinson, B. W., & Laberge, F. (2022). Evolutionary divergence in phenotypic plasticity shapes brain size variation between coexisting sunfish ecotypes. Journal of Evolutionary Biology, 35(10), 1363-1377. https://doi.org/10.1111/jeb.14085
Baldwin, J. M. (1896). A new factor in evolution. The American Naturalist, 30(354), 441-451. https://doi.org/10.1086/276408
Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(1), 1-48. https://doi.org/10.18637/jss.v067.i01
Battesti, M., Moreno, C., Joly, D., & Mery, F. (2012). Spread of social information and dynamics of social transmission within drosophila groups. Current Biology, 22(4), 309-313. https://doi.org/10.1016/j.cub.2011.12.050
Bertrand, O. C., Püschel, H. P., Schwab, J. A., Silcox, M. T., & Brusatte, S. L. (2021). The impact of locomotion on the brain evolution of squirrels and close relatives. Communications Biology, 4(1), 460. https://doi.org/10.1038/s42003-021-01887-8
Bogert, C. M. (1949). Thermoregulation in reptiles, a factor in evolution. Evolution, 3(3), 195-211. https://doi.org/10.2307/2405558
Broder, E. D. (2016). Evolution and plasticity of Trinidadian guppies in the field, the laboratory, and the classroom (Doctoral dissertation). Colorado State University. https://minerva-access.unimelb.edu.au/handle/11343/56627%0Ahttp://www.academia.edu/download/39541120/performance_culture.doc
Brown, G., & Chivers, D. (2005). Learning as an adaptive response to predation. In P. Barbosa & I. Castellanos (Eds.), Ecology of predator-prey interactions (pp. 34-54). Oxford University Press.
Cardoso, S. D., Teles, M. C., & Oliveira, R. F. (2015). Neurogenomic mechanisms of social plasticity. Journal of Experimental Biology, 218(1), 140-149. https://doi.org/10.1242/jeb.106997
Carroll, S. P., & Corneli, P. S. (1995). Divergence in male mating tactics between two populations of the soapberry bug: II. Genetic change and the evolution of a plastic reaction norm in a variable social environment. Behavioral Ecology, 6(1), 46-56. https://doi.org/10.1093/beheco/6.1.46
Cattelan, S., Evans, J. P., Pilastro, A., & Gasparini, C. (2016). The effect of sperm production and mate availability on patterns of alternative mating tactics in the guppy. Animal Behaviour, 112, 105-110. https://doi.org/10.1016/j.anbehav.2015.11.024
Chuard, P. J. C., Grant, J. W. A., Ramnarine, I. W., & Brown, G. E. (2020). Exploring the threat-sensitive predator avoidance hypothesis on mate competition in two wild populations of Trinidadian guppies. Behavioural Processes, 180(August), 104225. https://doi.org/10.1016/j.beproc.2020.104225
Coolen, I., Dangles, O., & Casas, J. (2005). Social learning in noncolonial insects? Current Biology, 15(21), 1931-1935. https://doi.org/10.1016/j.cub.2005.09.015
Crispo, E., Bentzen, P., Reznick, D. N., Kinnison, M. T., & Hendry, A. P. (2006). The relative influence of natural selection and geography on gene flow in guppies. Molecular Ecology, 15(1), 49-62. https://doi.org/10.1111/j.1365-294X.2005.02764.x
Cui, R., Delclos, P. J., Schumer, M., & Rosenthal, G. G. (2017). Early social learning triggers neurogenomic expression changes in a swordtail fish. Proceedings of the Royal Society B: Biological Sciences, 284(1854), 20170701. https://doi.org/10.1098/rspb.2017.0701
Devigili, A., Kelley, J. L., Pilastro, A., & Evans, J. P. (2013). Expression of pre-and postcopulatory traits under different dietary conditions in guppies. Behavioral Ecology, 24(3), 740-749. https://doi.org/10.1093/beheco/ars204
Dicke, U., & Roth, G. (2016). Neuronal factors determining high intelligence. Philosophical Transactions of the Royal Society B: Biological Sciences, 371(1685), 20150180. https://doi.org/10.1098/rstb.2015.0180
Dill, L. M., Hedrick, A. V., & Fraser, A. (1999). Male mating strategies under predation risk: Do females call the shots? Behavioral Ecology, 10(4), 452-461. https://doi.org/10.1093/beheco/10.4.452
Duckworth, R. A. (2009). The role of behavior in evolution: A search for mechanism. Evolutionary Ecology, 23(4), 513-531. https://doi.org/10.1007/s10682-008-9252-6
Duffy, J. A., & Hendricks, S. E. (1973). Influences of social isolation during development on sexual behavior of the rat. Animal Learning & Behavior, 1(3), 223-227. https://doi.org/10.3758/BF03199079
Dugatkin, L. A., & Godin, J.-G. (1992). Reversal of female mate choice by copying in the guppy (Poecilia reticulata). Proceedings of the Royal Society B: Biological Sciences, 249(1325), 179-184. https://doi.org/10.1098/rspb.1992.0101
Elvidge, C. K., Ramnarine, I., & Brown, G. E. (2014). Compensatory foraging in Trinidadian guppies: Effects of acute and chronic predation threats. Current Zoology, 60(3), 323-332. https://doi.org/10.1093/czoolo/60.3.323
Endler, J. A. (1978). A predator's view of animal color patterns. In M. K. Hecht, W. C. Steere, & B. Wallace (Eds.), Evolutionary biology (pp. 319-364). Springer US. https://doi.org/10.1007/978-1-4615-6956-5_5
Endler, J. A. (1980). Natural selection on color patterns in Poecilia reticulata. Evolution, 34(1), 76. https://doi.org/10.2307/2408316
Endler, J. A. (1995). Multiple-trait coevolution and environmental gradients in guppies. Trends in Ecology & Evolution, 10(1), 22-29. https://doi.org/10.1016/S0169-5347(00)88956-9
Endler, J. A., Butlin, R. K., Guilford, T., & Krebs, J. R. (1997). Some general comments on the evolution and design of animal communication systems. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 340(1292), 215-225. https://doi.org/10.1098/rstb.1993.0060
Evans, J. P. (2010). Quantitative genetic evidence that males trade attractiveness for ejaculate quality in guppies. Proceedings of the Royal Society B: Biological Sciences, 277(1697), 3195-3201. https://doi.org/10.1098/rspb.2010.0826
Evans, J. P., Kelley, J. L., Ramnarine, I. W., & Pilastro, A. (2002). Female behaviour mediates male courtship under predation risk in the guppy (Poecilia reticulata). Behavioral Ecology and Sociobiology, 52(6), 496-502. https://doi.org/10.1007/s00265-002-0535-6
Evans, J. P., & Magurran, A. E. (2001). Patterns of sperm precedence and predictors of paternity in the Trinidadian guppy. Proceedings of the Royal Society B: Biological Sciences, 268(1468), 719-724. https://doi.org/10.1098/rspb.2000.1577
Evans, J. P., Rahman, M. M., & Gasparini, C. (2015). Genotype-by-environment interactions underlie the expression of pre- and post-copulatory sexually selected traits in guppies. Journal of Evolutionary Biology, 28(4), 959-972. https://doi.org/10.1111/jeb.12627
Feldman, M. W., & Laland, K. N. (1996). Gene-culture coevolutionary theory. Trends in Ecology & Evolution, 11(11), 453-457. https://doi.org/10.1016/0169-5347(96)10052-5
Fischer, E. K., Ghalambor, C. K., & Hoke, K. L. (2016). Plasticity and evolution in correlated suites of traits. Journal of Evolutionary Biology, 29(5), 991-1002. https://doi.org/10.1111/jeb.12839
Fischer, E. K., Harris, R. M., Hofmann, H. A., & Hoke, K. L. (2014). Predator exposure alters stress physiology in guppies across timescales. Hormones and Behavior, 65(2), 165-172. https://doi.org/10.1016/j.yhbeh.2013.12.010
Fischer, E. K., Song, Y., Hughes, K. A., Zhou, W., & Hoke, K. L. (2021). Nonparallel transcriptional divergence during parallel adaptation. Molecular Ecology, 30(6), 1516-1530. https://doi.org/10.1111/mec.15823
Ghalambor, C. K., Hoke, K. L., Ruell, E. W., Fischer, E. K., Reznick, D. N., & Hughes, K. A. (2015). Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature. Nature, 525(7569), 372-375. https://doi.org/10.1038/nature15256
Ghalambor, C. K., McKay, J. K., Carroll, S. P., & Reznick, D. N. (2007). Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Functional Ecology, 21(3), 394-407. https://doi.org/10.1111/j.1365-2435.2007.01283.x
Glavaschi, A., Cattelan, S., Grapputo, A., & Pilastro, A. (2020). Imminent risk of predation reduces the relative strength of postcopulatory sexual selection in the guppy. Philosophical Transactions of the Royal Society B: Biological Sciences, 375(1813), 20200076. https://doi.org/10.1098/rstb.2020.0076
Godin, J. G. J. (1995). Predation risk and alternative mating tactics in male Trinidadian guppies (Poecilia reticulata). Oecologia, 103(2), 224-229. https://doi.org/10.1007/BF00329084
Godin, J. G. J., & McDonough, H. E. (2003). Predator preference for brightly colored males in the guppy: A viability cost for a sexually selected trait. Behavioral Ecology, 14(2), 194-200. https://doi.org/10.1093/beheco/14.2.194
Gonda, A., Herczeg, G., & Merilä, J. (2013). Evolutionary ecology of intraspecific brain size variation: A review. Ecology and Evolution, 3(8), 2751-2764. https://doi.org/10.1002/ece3.627
Griffin, A. S. (2004). Social learning about predators: A review and prospectus. Animal Learning & Behavior, 32(1), 131-140. https://doi.org/10.3758/BF03196014
Groemping, U., & Matthias, L. (2021). relaimpo: Relative importance of regressors in linear models (2.2-6) [Computer software]. https://CRAN.R-project.org/package=relaimpo
Guevara-Fiore, P. (2012). Early social experience significantly affects sexual behaviour in male guppies. Animal Behaviour, 84(1), 191-195. https://doi.org/10.1016/j.anbehav.2012.04.031
Guevara-Fiore, P., & Endler, J. A. (2018). Female receptivity affects subsequent mating effort and mate choice in male guppies. Animal Behaviour, 140, 73-79. https://doi.org/10.1016/j.anbehav.2018.04.007
Harris, R. M., & Hofmann, H. A. (2014). Neurogenomics of behavioral plasticity. In C. Landry & N. Aubin-Horth (Eds.), Ecological genomics (pp. 149-168). Springer. https://doi.org/10.1007/978-94-007-7347-9_8
Harrison, X. A. (2015). A comparison of observation-level random effect and Beta-binomial models for modelling overdispersion in binomial data in ecology & evolution. PeerJ, 2015(7), e1114. https://doi.org/10.7717/peerj.1114
Haskins, C. P., Haskins, E. F., McLaughlin, J. J. A., & Hewitt, R. E. (1961). Polymorphism and population structure in Lebistes reticulatus, an ecological study. In W. F. Blair (Ed.), Vertebrate speciation (pp. 320-395). University of Texas Press.
Heathcote, R. J. P., Darden, S. K., Franks, D. W., Ramnarine, I. W., & Croft, D. P. (2017). Fear of predation drives stable and differentiated social relationships in guppies. Scientific Reports, 7(May 2016), 1-10. https://doi.org/10.1038/srep41679
Herculano-Houzel, S. (2011). Not all brains are made the same: New views on brain scaling in evolution. Brain, Behavior and Evolution, 78(1), 22-36. https://doi.org/10.1159/000327318
Herculano-Houzel, S. (2017). Numbers of neurons as biological correlates of cognitive capability. Current Opinion in Behavioral Sciences, 16, 1-7. https://doi.org/10.1016/j.cobeha.2017.02.004
Herculano-Houzel, S., Mota, B., & Lent, R. (2006). Cellular scaling rules for rodent brains. Proceedings of the National Academy of Sciences of the United States of America, 103(32), 12138-12143. https://doi.org/10.1073/pnas.0604911103
Hesse, S., Bakker, T. C. M., Baldauf, S. A., & Thünken, T. (2016). Impact of social environment on inter- and intrasexual selection in a cichlid fish with mutual mate choice. Animal Behaviour, 111, 85-92. https://doi.org/10.1016/j.anbehav.2015.10.004
Hofman, M. A., & Falk, D. (2012). Evolution of the primate brain: From neuron to behavior (Vol. 195). Elsevier.
Jaatinen, K., Møller, A. P., & Öst, M. (2019). Annual variation in predation risk is related to the direction of selection for brain size in the wild. Scientific Reports, 9(1), 11847. https://doi.org/10.1038/s41598-019-48153-w
Kelley, J. L., Evans, J. P., Ramnarine, I. W., & Magurran, A. E. (2003). Back to school: Can antipredator behaviour in guppies be enhanced through social learning? Animal Behaviour, 65(4), 655-662. https://doi.org/10.1006/anbe.2003.2076
Kodric-Brown, A., & Nicoletto, P. F. (2001a). Age and experience affect female choice in the guppy (Poecilia reticulata). The American Naturalist, 157(3), 316-323. https://doi.org/10.1086/319191
Kodric-Brown, A., & Nicoletto, P. F. (2001b). Female choice in the guppy (Poecilia reticulata): The interaction between male color and display. Behavioral Ecology and Sociobiology, 50, 346-351. https://doi.org/10.1007/s002650100374
Kotrschal, A., Deacon, A. E., Magurran, A. E., & Kolm, N. (2017). Predation pressure shapes brain anatomy in the wild. Evolutionary Ecology, 31(5), 619-633. https://doi.org/10.1007/s10682-017-9901-8
Krause, J., Ruxton, G. D., Ruxton, G., & Ruxton, I. G. (2002). Living in groups. Oxford University Press.
Lefebvre, L., & Sol, D. (2008). Brains, lifestyles and cognition: Are there general trends? Brain, Behavior and Evolution, 72(2), 135-144. https://doi.org/10.1159/000151473
Lenth, R. V. (2022). emmeans: Estimated marginal means, aka least-squares means. R Package Version 1.7.3. https://cran.r-project.org/package=emmeans
Liley, N. R. (1966). Ethological isolating mechanisms in four sympatric species of Poeciliid fishes. Behaviour Supplement, 14, 1-197.
Luyten, P. H., & Liley, N. R. (1985). Geographic variation in the sexual behaviour of the guppy, Poecilia reticulata (Peters). Behaviour, 95(1-2), 164-179.
Magellan, K. I. T., & Magurran, A. E. (2007). Behavioural profiles: Individual consistency in male mating behaviour under varying sex ratios. Animal Behaviour, 74, 1545-1550. https://doi.org/10.1016/j.anbehav.2007.03.015
Magurran, A. E. (2001). Sexual conflict and evolution in Trinidadian guppies. Genetica, 112-113, 463-474. https://doi.org/10.1023/A:1013339822246
Magurran, A. E., & Nowak, M. A. (1991). Another battle of the sexes: The consequences of sexual asymmetry in mating costs and predation risk in the guppy, Poecilia reticulata. Proceedings of the Royal Society of London. Series B: Biological Sciences, 246(1315), 31-38. https://doi.org/10.1098/rspb.1991.0121
Magurran, A. E., & Seghers, B. H. (1990). Risk sensitive courtship in the guppy (Poecilia reticulata). Behaviour, 112(3-4), 194-201.
Marhounová, L., Kotrschal, A., Kverková, K., Kolm, N., & Němec, P. (2019). Artificial selection on brain size leads to matching changes in overall number of neurons. Evolution, 73(9), 2003-2012. https://doi.org/10.1111/evo.13805
Marler, P., & Tamura, M. (1964). Culturally transmitted patterns of vocal behavior in sparrows. Science, 146(3650), 1483-1486. https://doi.org/10.1126/science.146.3650.1483
Mayr, E. (1963). Animal species and evolution. Harvard University Press. https://doi.org/10.4159/harvard.9780674865327
Muñoz, M. M. (2022). The Bogert effect, a factor in evolution. Evolution, 76(Bogert 1949), 49-66. https://doi.org/10.1111/evo.14388
Pfennig, D. W. (2021). Phenotypic plasticity & evolution. CRC Press. https://doi.org/10.1201/9780429343001
Pike, T. W., Ramsey, M., & Wilkinson, A. (2018). Environmentally induced changes to brain morphology predict cognitive performance. Philosophical Transactions of the Royal Society B: Biological Sciences, 373(1756), 20170287. https://doi.org/10.1098/rstb.2017.0287
Pollen, A. A., Dobberfuhl, A. P., Scace, J., Igulu, M. M., Renn, S. C. P., Shumway, C. A., & Hofmann, H. A. (2007). Environmental complexity and social organization sculpt the brain in Lake Tanganyikan cichlid fish. Brain, Behavior and Evolution, 70(1), 21-39. https://doi.org/10.1159/000101067
Pusiak, R. J. P., Auld, H. L., & Godin, J.-G. J. (2020). Relative sexual attractiveness does not influence mate-choice copying in male Trinidadian guppies, Poecilia reticulata. Animal Behaviour, 162, 123-133. https://doi.org/10.1016/j.anbehav.2020.02.008
Pyter, L. M., Reader, B. F., & Nelson, R. J. (2005). Short photoperiods impair spatial learning and alter hippocampal dendritic morphology in adult male white-footed mice (Peromyscus leucopus). Journal of Neuroscience, 25(18), 4521-4526. https://doi.org/10.1523/JNEUROSCI.0795-05.2005
R Core Team. (2022). R: A language and environment for statistical computing [computer software]. R Foundation for Statistical Computing. https://www.r-project.org/
Reddon, A. R., Chouinard-Thuly, L., Leris, I., & Reader, S. M. (2018). Wild and laboratory exposure to cues of predation risk increases relative brain mass in male guppies. Functional Ecology, 32(7), 1847-1856. https://doi.org/10.1111/1365-2435.13128
Rodd, F. H., & Sokolowski, M. B. (1995). Complex origins of variation in the sexual behaviour of male trinidadian guppies, Poecilia reticulata: Interactions between social environment, heredity, body size and age. Animal Behaviour, 49(5), 1139-1159. https://doi.org/10.1006/anbe.1995.0149
Rosseel, Y., Jorgensen, T. D., Rockwood, N., Oberski, D., Byrnes, J., Vanbrabant, L., Savalei, V., Merkle, E., Hallquist, M., Rhemtulla, M., Katsikatsou, M., Barendse, M., Scharf, F., & Du, H. (2023). lavaan: Latent variable analysis (0.6-14). [computer software]. https://CRAN.R-project.org/package=lavaan
Sassi, P. L., Taraborelli, P., Albanese, S., & Gutierrez, A. (2015). Effect of temperature on activity patterns in a small andean rodent: Behavioral plasticity and intraspecific variation. Ethology, 121(9), 840-849.
Schlichting, C. D., & Pigliucci, M. (1998). Phenotypic evolution: A reaction norm perspective. Sinauer Associates Incorporated.
Schumacher, E. L., & Carlson, B. A. (2022). Convergent mosaic brain evolution is associated with the evolution of novel electrosensory systems in teleost fishes. eLife, 11, e74159. https://doi.org/10.7554/eLife.74159
Seghers, B. H., & Magurran, A. E. (1991). Variation in schooling and aggression amongst guppy (Poecilia Reticulata) populations in Trinidad. Behaviour, 118(3-4), 214-234. https://doi.org/10.1163/156853991X00292
Shumway, C. A. (2010). The evolution of complex brains and behaviors in African cichlid fishes. Current Zoology, 56(1), 144-156. https://doi.org/10.1093/czoolo/56.1.144
Simpson, G. G. (1953). The Baldwin effect. Evolution, 7(2), 110. https://doi.org/10.2307/2405746
Snell-Rood, E. C. (2013). An overview of the evolutionary causes and consequences of behavioural plasticity. Animal Behaviour, 85(5), 1004-1011. https://doi.org/10.1016/j.anbehav.2012.12.031
Stephenson, J. F. (2016). Keeping eyes peeled: Guppies exposed to chemical alarm cue are more responsive to ambiguous visual cues. Behavioral Ecology and Sociobiology, 70(4), 575-584. https://doi.org/10.1007/s00265-016-2076-4
Tollrian, R., & Harvell, C. D. (1999). The ecology and evolution of inducible defenses. Princeton University Press.
Travis, J., Reznick, D., Bassar, R. D., López-Sepulcre, A., Ferriere, R., & Coulson, T. (2014). Do eco-evo feedbacks help us understand nature? Answers from studies of the Trinidadian guppy. Advances in Ecological Research, 50, 1-40. https://doi.org/10.1016/B978-0-12-801374-8.00001-3
Van Buskirk, J. (2002). A comparative test of the adaptive plasticity hypothesis: Relationships between habitat and phenotype in anuran larvae. The American Naturalist, 160(1), 87-102. https://doi.org/10.1086/340599
van der Bijl, W., & Kolm, N. (2016). Why direct effects of predation complicate the social brain hypothesis. BioEssays, 38(6), 568-577. https://doi.org/10.1002/bies.201500166
Ward, A. J. W., & Mehner, T. (2010). Multimodal mixed messages: The use of multiple cues allows greater accuracy in social recognition and predator detection decisions in the mosquitofish, Gambusia holbrooki. Behavioral Ecology, 21(6), 1315-1320. https://doi.org/10.1093/beheco/arq152
West-Eberhard, M. J. (2003). Developmental plasticity and evolution. Oxford University Press.
Westneat, D. F., Potts, L. J., Sasser, K. L., & Shaffer, J. D. (2019). Causes and consequences of phenotypic plasticity in complex environments. Trends in Ecology & Evolution, 34(6), 555-568. https://doi.org/10.1016/j.tree.2019.02.010
White, G. E., & Brown, C. (2015). Variation in brain morphology of intertidal gobies: A comparison of methodologies used to quantitatively assess brain volumes in fish. Brain, Behavior and Evolution, 85(4), 245-256. https://doi.org/10.1159/000398781
Whiten, A., Goodall, J., McGrew, W. C., Nishida, T., Reynolds, V., Sugiyama, Y., Tutin, C. E. G., Wrangham, R. W., & Boesch, C. (1999). Cultures in chimpanzees. Nature, 399(6737), 682-685. https://doi.org/10.1038/21415
Wright, J., Haaland, T. R., Dingemanse, N. J., & Westneat, D. F. (2022). A reaction norm framework for the evolution of learning: How cumulative experience shapes phenotypic plasticity. Biological Reviews, 97(5), 1999-2021. https://doi.org/10.1111/brv.12879
Yang, Y., Axelrod, C. J., Grant, E., Earl, S., Urquhart, E., Talbert, K., Johnson, L., Walker, Z., Hsiao, K., Stone, I., Carlson, B. A., Lopez-Sepulcre, A., & Gordon, S. P. (2023). Data for: Evolutionary divergence of developmental plasticity and learning of mating strategies in Trinidadian guppies [dataset]. Dryad Digital Repository, https://doi.org/10.5061/dryad.2z34tmpsr
Yang, Y., Grant, E., López-Sepulcre, A., & Gordon, S. P. (2023). Female foraging strategy co-evolves with sexual harassment intensity in the Trinidadian guppy. Behavioral Ecology, 34, 593-601. https://doi.org/10.1093/beheco/arad027
Yong, L., Croft, D. P., Troscianko, J., Ramnarine, I. W., & Wilson, A. J. (2022). Sensory-based quantification of male colour patterns in Trinidadian guppies reveals no support for parallel phenotypic evolution in multivariate trait space. Molecular Ecology, 31(5), 1337-1357. https://doi.org/10.1111/mec.16039
Zupanc, G. K. H., & Lamprecht, J. (2000). Towards a cellular understanding of motivation: Structural reorganization and biochemical switching as key mechanisms of behavioral plasticity. Ethology, 106(5), 467-477. https://doi.org/10.1046/j.1439-0310.2000.00546.x