Predator exposure early in life shapes behavioral development and individual variation in a clonal fish.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
17 Sep 2024
17 Sep 2024
Historique:
received:
20
02
2024
accepted:
09
09
2024
medline:
18
9
2024
pubmed:
18
9
2024
entrez:
17
9
2024
Statut:
epublish
Résumé
Predation risk is one of the most important factors generating behavioral differences among populations. In addition, recent attention focusses on predation as a potential driver of patterns of individual behavioral variation within prey populations. Previous studies provide mixed results, reporting either increased or decreased among-individual variation in response to risk. Here, we take an explicit developmental approach to documenting how among-individual variation develops over time in response to predator exposure, controlling for both genetic and experiential differences among individuals. We reared juveniles of naturally clonal Amazon mollies, Poecilia formosa, either with or without a predator visible during feedings over 4 weeks and analyzed activity during feedings, time spent feeding and number of visits to the feeding spot. (I) Predator-exposed fish did not differ from control fish in average feeding behavior, but they were less active during feeding trials. (II) In the absence of the predator, substantial changes in among-individual variation over time were detected: among-individual differences in feeding duration increased whereas differences in activity decreased, but there were no changes in feeder visits. In contrast, in the presence of a predator, among-individual variation in all three behaviors was stable over time and often lower compared to control conditions. Our work suggests that predation risk may have an overall stabilizing effect on the development of individual variation and that differences in predation risk may well lead to population-wide differences in among-individual behavioral variation.
Identifiants
pubmed: 39289453
doi: 10.1038/s41598-024-72550-5
pii: 10.1038/s41598-024-72550-5
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
21668Subventions
Organisme : Deutsche Forschungsgemeinschaft
ID : EXC 2002/1, "Science of Intelligence" project number 390523135
Organisme : Deutsche Forschungsgemeinschaft
ID : BI 1828/2-1
Organisme : Deutsche Forschungsgemeinschaft
ID : BI 1828/2-1
Organisme : Deutsche Forschungsgemeinschaft
ID : EXC 2002/1, "Science of Intelligence" project number 390523135
Organisme : Deutsche Forschungsgemeinschaft
ID : EXC 2002/1, "Science of Intelligence" project number 390523135
Organisme : Deutsche Forschungsgemeinschaft
ID : EXC 2002/1, "Science of Intelligence" project number 390523135
Informations de copyright
© 2024. The Author(s).
Références
Sosna, M. M. G. et al. Individual and collective encoding of risk in animal groups. Proc. Natl. Acad. Sci. 116, 20556–20561 (2019).
pubmed: 31548427
pmcid: 6789631
doi: 10.1073/pnas.1905585116
Doran, C. et al. Fish waves as emergent collective antipredator behavior. Curr. Biol. 32, 708-714.e4 (2022).
pubmed: 34942081
doi: 10.1016/j.cub.2021.11.068
Bierbach, D. et al. Predator-induced changes of female mating preferences: Innate and experiential effects. BMC Evol. Biol 11, 190 (2011).
pubmed: 21726456
pmcid: 3141438
doi: 10.1186/1471-2148-11-190
Sih, A. Predation risk and the evolutionary ecology of reproductive behaviour. J. Fish Biol. 45, 111–130 (1994).
doi: 10.1111/j.1095-8649.1994.tb01087.x
Walls, M., Kortelainen, I. & Sarvala, J. Prey responses to fish predation in freshwater communities. Ann. Zool. Fennici. 27, 183–199 (1990).
Lima, S. L. & Dill, L. M. Behavioral decisions made under the risk of predation: a review and prospectus. Can. J. Zool. 68, 619–640 (1990).
doi: 10.1139/z90-092
Gabor, C., Coyle, J. & Aspbury, A. Effect of predation on male mating behaviour in a unisexual-bisexual mating system. Behaviour 147, 53–63 (2010).
doi: 10.1163/000579509X12483520922160
Brown, C., Burgess, F. & Braithwaite, V. A. Heritable and experiential effects on boldness in a tropical poeciliid. Behav. Ecol. Sociobiol. 62, 237–243 (2007).
doi: 10.1007/s00265-007-0458-3
Harris, S. et al. Picking personalities apart: estimating the influence of predation, sex and body size on boldness in the guppy Poecilia reticulata. Oikos 119, 1711–1718 (2010).
doi: 10.1111/j.1600-0706.2010.18028.x
Archard, G. A. & Braithwaite, V. A. Increased exposure to predators increases both exploration and activity level in Brachyrhaphis episcopi. J. Fish Biol. 78, 593–601 (2011).
pubmed: 21284637
doi: 10.1111/j.1095-8649.2010.02880.x
Brown, C., Jones, F. & Braithwaite, V. In situ examination of boldness–shyness traits in the tropical poeciliid Brachyraphis episcopi. Anim. Behav. 70, 1003–1009 (2005).
doi: 10.1016/j.anbehav.2004.12.022
Catano, L. B. et al. Reefscapes of fear: predation risk and reef heterogeneity interact to shape herbivore foraging behaviour. J. Anim. Ecol. 85, 146–156 (2016).
pubmed: 26332988
doi: 10.1111/1365-2656.12440
Bolnick, D. I. et al. Why intraspecific trait variation matters in community ecology. Trends Ecol. Evol. 26, 183–192 (2011).
pubmed: 21367482
pmcid: 3088364
doi: 10.1016/j.tree.2011.01.009
Wolf, M. & Weissing, F. J. Animal personalities: Consequences for ecology and evolution. Trends Ecol. Evol. 27, 452–461 (2012).
pubmed: 22727728
doi: 10.1016/j.tree.2012.05.001
Carere, C. & Gherardi, F. Animal personalities matter for biological invasions. Trends Ecol. Evol. 28, 5–6 (2013).
pubmed: 23131537
doi: 10.1016/j.tree.2012.10.006
Ingley, S. J. & Johnson, J. B. Animal personality as a driver of reproductive isolation. Trends Ecol. Evol. 29, 369–371 (2014).
pubmed: 24837793
doi: 10.1016/j.tree.2014.04.008
Réale, D. et al. Integrating animal temperament within ecology and evolution. Biol. Rev. 82, 291–318 (2007).
pubmed: 17437562
doi: 10.1111/j.1469-185X.2007.00010.x
Bell, A. M., Hankison, S. J. & Laskowski, K. L. The repeatability of behaviour: a meta-analysis. Anim. Behav. 77, 771–783 (2009).
pubmed: 24707058
pmcid: 3972767
doi: 10.1016/j.anbehav.2008.12.022
Blake, C. A. & Gabor, C. R. Effect of prey personality depends on predator species. Behav. Ecol. 25, 871–877 (2014).
doi: 10.1093/beheco/aru041
Dammhahn, M. & Almeling, L. Is risk taking during foraging a personality trait? A field test for cross-context consistency in boldness. Anim. Behav. 84, 1131–1139 (2012).
doi: 10.1016/j.anbehav.2012.08.014
Toscano, B. J., Gatto, J. & Griffen, B. D. Effect of predation threat on repeatability of individual crab behavior revealed by mark-recapture. Behav. Ecol. Sociobiol. 68, 519–527 (2014).
doi: 10.1007/s00265-013-1666-7
Ehlman, S. M. et al. Intermediate turbidity elicits the greatest antipredator response and generates repeatable behaviour in mosquitofish. Anim. Behav. 158, 101–108 (2019).
doi: 10.1016/j.anbehav.2019.10.006
Mitchell, D. J., Beckmann, C. & Biro, P. Maintenance of behavioral variation under predation risk: effects on personality, plasticity, and predictability. Am. Nat. https://doi.org/10.1086/728421 (2023).
Urszán, T. J. et al. No personality without experience? A test on Rana dalmatina tadpoles. Ecol. Evol. 5, 5847–5856 (2015).
pubmed: 26811759
pmcid: 4717344
doi: 10.1002/ece3.1804
Bell, A. M. & Sih, A. Exposure to predation generates personality in three-spined sticklebacks (Gasterosteus aculeatus). Ecol. Lett. 10, 828–834 (2007).
pubmed: 17663716
doi: 10.1111/j.1461-0248.2007.01081.x
Dingemanse, N. J. et al. Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J. Anim. Ecol. 76, 1128–1138 (2007).
pubmed: 17922709
doi: 10.1111/j.1365-2656.2007.01284.x
Muraco, J. J. et al. Do females in a unisexual-bisexual species complex differ in their behavioral syndromes and cortisol production?. Biology (Basel) 10, 186 (2021).
pubmed: 33802259
Muraco, J. J., Aspbury, A. S. & Gabor, C. R. Does male behavioral type correlate with species recognition and stress?. Behav. Ecol. 25, 200–205 (2014).
doi: 10.1093/beheco/art106
Dingemanse, N. J. et al. Individual experience and evolutionary history of predation affect expression of heritable variation in fish personality and morphology. Proc. R. Soc. B: Biol. Sci. 276, 1285–1293 (2009).
doi: 10.1098/rspb.2008.1555
Sommer-Trembo, C. et al. Predator experience homogenizes consistent individual differences in predator avoidance. J. Ethol. 34, 155–165 (2016).
doi: 10.1007/s10164-016-0460-1
Castellano, S. & Friard, O. Environmental effects on the ontogenesis of tadpole personality. Anim. Behav. 175, 153–161 (2021).
doi: 10.1016/j.anbehav.2021.03.002
Kelley, J. L. & Magurran, A. E. Learned predator recognition and antipredator responses in fishes. Fish Fish. 4, 216–226 (2003).
doi: 10.1046/j.1467-2979.2003.00126.x
Tulley, J. J. & Huntingford, F. A. Age, experience and the development of adaptive variation in anti-predator responses in three-spined sticklebacks (Gasterosteus aculeatus). Ethology 75, 285–290 (1987).
doi: 10.1111/j.1439-0310.1987.tb00660.x
Toscano, B. J. et al. Among-individual behavioral responses to predation risk are invariant within two species of freshwater snails. Ethology 129, 269–279 (2023).
doi: 10.1111/eth.13363
Carlson, B. A. Early life experiences have complex and long-lasting effects on behavior. Proc. Natl. Acad. Sci. 114, 11571–11573 (2017).
pubmed: 29078413
pmcid: 5676937
doi: 10.1073/pnas.1716037114
Crane, A. L. et al. Early-life and parental predation risk shape fear acquisition in adult minnows. Anim. Cogn. 24, 471–481 (2021).
pubmed: 33125574
doi: 10.1007/s10071-020-01439-3
Jonsson, B. & Jonsson, N. Early environment influences later performance in fishes. J. Fish Biol. 85, 151–188 (2014).
pubmed: 24961386
doi: 10.1111/jfb.12432
Barbosa, M. et al. Individual variation in reproductive behaviour is linked to temporal heterogeneity in predation risk. Proc. R. Soc. B: Biol. Sci. 285, 20171499 (2018).
doi: 10.1098/rspb.2017.1499
Polverino, G. et al. Ecological conditions drive pace-of-life syndromes by shaping relationships between life history, physiology and behaviour in two populations of Eastern mosquitofish. Sci. Rep. 8, 14673 (2018).
pubmed: 30279465
pmcid: 6168454
doi: 10.1038/s41598-018-33047-0
Stamps, J. A. & Biro, P. A. Time-specific convergence and divergence in individual differences in behavior: Theory, protocols and analyzes. Ecol. Evol. https://doi.org/10.1002/ece3.10615 (2023).
pubmed: 38034332
pmcid: 10682899
Ehlman, S., Scherer, U. & Wolf, M. Developmental feedbacks and the emergence of individuality. R. Soc. Open Sci. 9, 221189 (2022).
pubmed: 36465682
pmcid: 9709565
doi: 10.1098/rsos.221189
Ehlman, S. M. et al. Leveraging big data to uncover the eco-evolutionary factors shaping behavioural development. Proc. R. Soc. B 290, 20222115 (2023).
pubmed: 36722081
pmcid: 9890127
doi: 10.1098/rspb.2022.2115
Laskowski, K. L. et al. Naturally clonal vertebrates are an untapped resource in ecology and evolution research. Nat. Ecol. Evol. 3, 161–169 (2019).
pubmed: 30692622
doi: 10.1038/s41559-018-0775-0
Biro, P. A. & Stamps, J. A. Using repeatability to study physiological and behavioural traits: ignore time-related change at your peril. Anim. Behav. 105, 223–230 (2015).
doi: 10.1016/j.anbehav.2015.04.008
Dingemanse, N. J. & Dochtermann, N. A. Quantifying individual variation in behaviour: Mixed-effect modelling approaches. J. Anim. Ecol. 82, 39–54 (2013).
pubmed: 23171297
doi: 10.1111/1365-2656.12013
Bierbach, D., Laskowski, K. L. & Wolf, M. Behavioural individuality in clonal fish arises despite near-identical rearing conditions. Nat. Commun. 8, 15361 (2017).
pubmed: 28513582
pmcid: 5442312
doi: 10.1038/ncomms15361
Laskowski, K. L. et al. The emergence and development of behavioral individuality in clonal fish. Nat. Commun. 13, 6419 (2022).
pubmed: 36307437
pmcid: 9616841
doi: 10.1038/s41467-022-34113-y
Scherer, U. et al. Reproductive individuality of clonal fish raised in near-identical environments and its link to early-life behavioral individuality. Nat. Commun. 14, 7652 (2023).
pubmed: 38001119
pmcid: 10673926
doi: 10.1038/s41467-023-43069-6
Wooster, D. & Sih, A. A review of the drift and activity responses of stream prey to predator presence. Oikos 73, 3 (1995).
doi: 10.2307/3545718
Lima, S. L. & Bednekoff, P. A. Temporal variation in danger drives antipredator behavior: The predation risk allocation hypothesis. Am. Nat. 153, 249–259 (1999).
doi: 10.1086/303202
Scherer, U., Godin, J.-G.J. & Schuett, W. Validation of 2D-animated pictures as an investigative tool in the behavioural sciences: A case study with a West African cichlid fish, Pelvicachromis pulcher. Ethology https://doi.org/10.1111/eth.12630 (2017).
O’Connor, C. M. et al. Social cichlid fish change behaviour in response to a visual predator stimulus, but not the odour of damaged conspecifics. Behav. Process. 121, 21–29 (2015).
doi: 10.1016/j.beproc.2015.10.002
Milinski M. Constraints placed by predators on feeding behaviour. In: The Behaviour of Teleost Fishes. Boston, MA: Springer US, 1986, pp. 236–252.
Cooper, W. E. & Blumstein, D. T. Escaping from predators (Cambridge University Press, 2015).
doi: 10.1017/CBO9781107447189
Bierbach, D. et al. Predator avoidance in extremophile fish. Life 3, 161–180 (2013).
pubmed: 25371337
pmcid: 4187198
doi: 10.3390/life3010161
Hawkins, Magurran, Armstrong. Innate predator recognition in newly-hatched Atlantic salmon. Behaviour 141, 1249–1262 (2004).
Culumber, Z. W. Early recognition and response to predator, heterospecific, and conspecific visual cues by multiple species of poeciliid fry. Behaviour 152, 1463–1479 (2015).
doi: 10.1163/1568539X-00003287
Plath, M. et al. Predator-induced changes of male and female mating preferences: innate and learned components. Curr. Zool. 65, 305–316 (2019).
pubmed: 31263489
pmcid: 6595919
doi: 10.1093/cz/zoz003
Karplus, I. & Algom, D. Visual cues for predator face recognition by reef fishes. Z. Tierpsychol. 55, 343–364 (1981).
doi: 10.1111/j.1439-0310.1981.tb01277.x
Kelley, J. L. & Magurran, A. E. Effects of relaxed predation pressure on visual predator recognition in the guppy. Behav. Ecol. Sociobiol. 54, 225–232 (2003).
doi: 10.1007/s00265-003-0621-4
Smith, J. M. & Brown, R. L. W. Competition and body size. Theor. Popul. Biol. 30, 166–179 (1986).
pubmed: 3787500
doi: 10.1016/0040-5809(86)90031-6
Buston, P. M. & Cant, M. A. A new perspective on size hierarchies in nature: Patterns, causes, and consequences. Oecologia 149, 362–372 (2006).
pubmed: 16794835
doi: 10.1007/s00442-006-0442-z
Bisazza, A. & Marconato, A. Female mate choice, male-male competition and parental care in the river bullhead, Cottus gobio L. (Pisces, Cottidae). Anim. Behav. 36, 1352–1360 (1988).
doi: 10.1016/S0003-3472(88)80204-5
Landeau, L. & Terborgh, J. Oddity and the ‘confusion effect’ in predation. Anim. Behav. 34, 1372–1380 (1986).
doi: 10.1016/S0003-3472(86)80208-1
Crane, A. L. et al. Uncertainty about predation risk: a conceptual review. Biol. Rev. https://doi.org/10.1111/brv.13019 (2023).
pubmed: 37839808
Sih, A. Prey uncertainty and the balancing of antipredator and feeding needs. Am. Nat. 139, 1052–1062 (1992).
doi: 10.1086/285372
Sih, A. et al. Animal personality and state–behaviour feedbacks: A review and guide for empiricists. Trends Ecol. Evol. 30, 50–60 (2015).
pubmed: 25498413
doi: 10.1016/j.tree.2014.11.004
Lamatsch, D. K., Schmid, M. & Schartl, M. A somatic mosaic of the gynogenetic Amazon molly. J. Fish Biol. 60, 1417–1422 (2005).
doi: 10.1111/j.1095-8649.2002.tb02436.x
Lampert, K. P. & Schartl, M. The origin and evolution of a unisexual hybrid: Poecilia formosa. Phil. Trans. R. Soc. B: Biol. Sci. 363, 2901–2909 (2008).
doi: 10.1098/rstb.2008.0040
Schlupp, I. The evolutionary ecology of gynogenesis. Annu. Rev. Ecol. Evol. Syst. 36, 399–417 (2005).
doi: 10.1146/annurev.ecolsys.36.102003.152629
Stöck, M. et al. Monophyletic origin of multiple clonal lineages in an asexual fish (Poecilia formosa). Mol. Ecol. 19, 5204–5215 (2010).
pubmed: 20964758
doi: 10.1111/j.1365-294X.2010.04869.x
Warren, W. C. et al. Clonal polymorphism and high heterozygosity in the celibate genome of the Amazon molly. Nat. Ecol. Evol. 2, 669–679 (2018).
pubmed: 29434351
pmcid: 5866774
doi: 10.1038/s41559-018-0473-y
Hubbs, C. L. & Hubbs, L. C. Apparent parthenogenesis in nature, in a form of fish of hybrid origin. Science 1932(76), 628–630 (1979).
Schultz, R. J. Origin and synthesis of a unisexual fish. In Genetics and Mutagenesis of Fish (ed. Schröder, J. H.) 207–211 (Springer, Berlin, Heidelberg, 1973).
doi: 10.1007/978-3-642-65700-9_20
Alberici da Barbiano, L. et al. Population genomics reveals a possible history of backcrossing and recombination in the gynogenetic fish Poecilia formosa. Proc. Natl. Acad. Sci. 110, 13797–13802 (2013).
pubmed: 23918384
pmcid: 3752203
doi: 10.1073/pnas.1303730110
Kallman, K. D. Gynogenesis in the teleost, Mollienesia formosa (Girard), with a discussion of the detection of parthenogenesis in vertebrates by tissue transplantation. J. Genet. 58(1), 7–24 (1962).
doi: 10.1007/BF02986114
Rasch, E. M. et al. Cytophotometric evidence for triploidy in hybrids of the gynogenetic fish, Poecilia formosa. J. Exp. Zool. 160, 155–169 (1965).
pubmed: 5894252
doi: 10.1002/jez.1401600203
Turner, B. J. et al. Evolutionary genetics of a gynogenetic fish, Poecilia formosa, the Amazon molly. Evolution (NY) 34, 246 (1980).
Lu, Y. et al. Fixation of allelic gene expression landscapes and expression bias pattern shape the transcriptome of the clonal Amazon molly. Genome Res. 31, 372–379 (2021).
pubmed: 33547183
pmcid: 7919451
doi: 10.1101/gr.268870.120
Lukas, J. A. Y. et al. On the occurrence of three non-native cichlid species including the first record of a feral population of Pelmatolapia (Tilapia) mariae (Boulenger, 1899) in Europe. R. Soc. Open Sci. 4, 170160 (2017).
pubmed: 28680671
pmcid: 5493913
doi: 10.1098/rsos.170160
R Core Team. R: A language and environment for statistical computing.
Bates, D., Mächler, M. & Bolker, B. Fitting linear mixed-effects models using the lme4 package in R. J. Stat. Softw. 67, 1–48 (2015).
doi: 10.18637/jss.v067.i01
Hertel, A. G. et al. A guide for studying among-individual behavioral variation from movement data in the wild. Mov. Ecol. 8, 30 (2020).
pubmed: 32612837
pmcid: 7325061
doi: 10.1186/s40462-020-00216-8