Model and Data Concur and Explain the Coexistence of Two Very Distinct Animal Behavioral Types

. 2020 Aug 21 ; 9 (9) : . [epub] 20200821

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid32825577

Grantová podpora
CGL2004-03153 Ministerio de Ciencia y Tecnología

Behaviors may enhance fitness in some situations while being detrimental in others. Linked behaviors (behavioral syndromes) may be central to understanding the maintenance of behavioral variability in natural populations. The spillover hypothesis of premating sexual cannibalism by females explains genetically determined female aggression towards both prey and males: growth to a larger size translates into higher fecundity, but at the risk of insufficient sperm acquisition. Here, we use an individual-based model to determine the ecological scenarios under which this spillover strategy is more likely to evolve over a strategy in which females attack approaching males only once the female has previously secured sperm. We found that a classic spillover strategy could never prevail. However, a more realistic early-spillover strategy, in which females become adults earlier in addition to reaching a larger size, could be maintained in some ecological scenarios and even invade a population of females following the other strategy. We also found under some ecological scenarios that both behavioral types coexist through frequency-dependent selection. Additionally, using data from the spider Lycosa hispanica, we provide strong support for the prediction that the two strategies may coexist in the wild. Our results clarify how animal personalities evolve and are maintained in nature.

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Lande R. Natural Selection and Random Genetic Drift in Phenotypic Evolution. Evolution. 1976;30:314–334. doi: 10.1111/j.1558-5646.1976.tb00911.x. PubMed DOI

West-Eberhard M. Developmental Plasticity and Evolution. Oxford University Press; New York, NY, USA: 2003.

Bolnick D., Svanbäck R., Fordyce J., Yang L., Davis J., Hulsey C., Forister M. The Ecology of Individuals: Incidence and Implications of Individual Specialization. Am. Nat. 2003;161:1–28. doi: 10.1086/343878. PubMed DOI

Bolnick D., Amarasekare P., Araújo M., Bürger R., Levine J., Novak M., Rudolf V., Schreiber S., Urban M., Vasseur D. Why intraspecific trait variation matters in community ecology. Trends Ecol. Evol. 2011;26:183–192. doi: 10.1016/j.tree.2011.01.009. PubMed DOI PMC

Des Roches S., Post D., Turley N., Bailey J., Hendry A., Kinnison M., Schweitzer J., Palkovacs E. The ecological importance of intraspecific variation. Nat. Ecol. Evol. 2018;2 doi: 10.1038/s41559-017-0402-5. PubMed DOI

Raffard A., Santoul F., Cucherousset J., Blanchet S. The community and ecosystem consequences of intraspecific diversity: A meta-analysis. Biol. Rev. 2018;94 doi: 10.1111/brv.12472. PubMed DOI

Moya-Laraño J., Bilbao-Castro J., Barrionuevo Rosales G., Ruiz-Lupión D., Casado L.G., Montserrat M., Melian C., Magalhaes S. Eco-Evolutionary Spatial Dynamics: Rapid Evolution and Isolation Explain Food Web Persistence. Adv. Ecol. Res. 2014;50:75–143. doi: 10.1016/B978-0-12-801374-8.00003-7. DOI

Schoener T. The Newest Synthesis: Understanding the Interplay of Evolutionary and Ecological Dynamics. Science. 2011;331:426–429. doi: 10.1126/science.1193954. PubMed DOI

Yoshida T., Ellner S., Jones L., Bohannan B., Lenski R., Hairston N. Cryptic Population Dynamics: Rapid Evolution Masks Trophic Interactions. PLoS Biol. 2007;5:e235. doi: 10.1371/journal.pbio.0050235. PubMed DOI PMC

Roff D. Evolutionary Quantitative Genetics. Volume 2. Springer US; New York, NY, USA: 1997. Evolutionary Quantitative Genetic; p. 493.

Dingemanse N., Wolf M. Between-individual differences in behavioural plasticity within populations: Causes and consequences. Anim. Behav. 2013;85:1031–1039. doi: 10.1016/j.anbehav.2012.12.032. DOI

Sih A., Bell A., Johnson J., Robert Z. Behavioral syndromes: An integrative overview. Q. Rev. Biol. 2004;79:241–277. doi: 10.1086/422893. PubMed DOI

Sih A., Bell A., Johnson J. Behavioral syndrome: An ecological and evolutionary overview. Trends Ecol. Evol. 2004;19:372–378. doi: 10.1016/j.tree.2004.04.009. PubMed DOI

Bell A. Future directions in behavioural syndromes research. Proc. Biol. Sci. 2007;274:755–761. doi: 10.1098/rspb.2006.0199. PubMed DOI PMC

Sih A., Cote J., Evans M., Fogarty S., Pruitt J. Ecological implications of behavioural syndromes. Ecol. Lett. 2012;15:278–289. doi: 10.1111/j.1461-0248.2011.01731.x. PubMed DOI

Wolf M., Weissing F. Animal personalities: Consequences for ecology and evolution. Trends Ecol. Evol. 2012;27:452–461. doi: 10.1016/j.tree.2012.05.001. PubMed DOI

Réale D., Reader S., Sol D., McDougall P., Dingemanse N. Integrating animal temperament within ecology and evolution. Biol. Rev. Camb. Philos. Soc. 2007;82:291–318. doi: 10.1111/j.1469-185X.2007.00010.x. PubMed DOI

Réale D., Garant D., Humphries M., Bergeron P., Careau V., Montiglio P.-O. Personality and the emergence of the pace-of-life syndrome concept at the population level. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2010;365:4051–4063. doi: 10.1098/rstb.2010.0208. PubMed DOI PMC

Maynard-Smith J. Evolution and the Theory of Games. Cambridge University Press; Cambridge, UK: 1982.

Maynard-Smith J., Harper D. The Evolution of Aggression: Can Selection Generate Variability? [and Discussion] Philos. Trans. R. Soc. Lond. B Biol. Sci. 1988;319:557–570. doi: 10.1098/rstb.1988.0065. PubMed DOI

Wolf M., van Doorn S., Weissing F. Evolutionary emergence of responsive and unresponsive personalities.Evolutionary emergence of responsive and unresponsive personalities. Proc. Natl. Acad. Sci. USA. 2008;105:15825–15830. doi: 10.1073/pnas.0805473105. PubMed DOI PMC

Wolf M., Mcnamara J., Wolf M., McNamara J.M. On the evolution of personalities via frequency-dependent selection. Am. Nat. 2012;179:679–692. doi: 10.1086/665656. PubMed DOI

Wolf M., Weissing F. An explanatory framework for adaptive personality differences. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2010;365:3959–3968. doi: 10.1098/rstb.2010.0215. PubMed DOI PMC

Bell A. Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus) J. Evol. Biol. 2005;18:464–473. doi: 10.1111/j.1420-9101.2004.00817.x. PubMed DOI

Dingemanse N., Wright J., Kazem A., Thomas D., Hickling R., Dawnay N. Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J. Anim. Ecol. 2007;76:1128–1138. doi: 10.1111/j.1365-2656.2007.01284.x. PubMed DOI

Dingemanse N., Kazem A., Réale D., Wright J. Behavioural reaction norms: Animal personality meets individual plasticity. Trends Ecol. Evol. 2010;25:81–89. doi: 10.1016/j.tree.2009.07.013. PubMed DOI

Dingemanse N., Bouwman K., van de Pol M., Overveld T., Patrick S., Matthysen E., Quinn J. Variation in personality and behavioural plasticity across four populations of the great tit Parus major. J. Anim. Ecol. 2012;81:116–126. doi: 10.1111/j.1365-2656.2011.01877.x. PubMed DOI

Elgar M. Cannibalism: Ecology and Evolution among Diverse Taxa. Oxford University Press; Oxford, UK: 1992. Sexual cannibalism in spiders and other invertebrates.

Elgar M., Schneider J. Advances in The Study of Behavior. Volume 34. Elsevier; Amsterdam, The Netherlands: 2004. Evolutionary Significance of Sexual Cannibalism; pp. 135–163.

Arnqvist G., Henriksson S. Sexual cannibalism in fishing spider and a model for the evolution of sexual cannibalism based on genetic constraints. Evol. Ecol. 1997;11:255–273. doi: 10.1023/A:1018412302621. DOI

Johnson J., Sih A. Fear, food, sex and parental care: A syndrome of boldness in the fishing spider, Dolomedes triton. Anim. Behav. 2007;74:1131–1138. doi: 10.1016/j.anbehav.2007.02.006. DOI

Johnson J., Sih A. Precopulatory sexual cannibalism in fishing spiders (Dolomedes triton): A role for behavioral syndromes. Behav. Ecol. Sociobiol. 2005;58:390–396. doi: 10.1007/s00265-005-0943-5. DOI

Kralj-Fišer S., Schneider J., Kuntner M., Hauber M. Challenging the Aggressive Spillover Hypothesis: Is Pre-Copulatory Sexual Cannibalism a Part of a Behavioural Syndrome? Ethology. 2013;119 doi: 10.1111/eth.12111. DOI

Moya-Laraño J., Pascual J., Wise D. Mating patterns in late-maturing female Mediterranean tarantulas may reflect the costs and benefits of sexual cannibalism. Anim. Behav. 2003;66:469–476. doi: 10.1006/anbe.2003.2262. DOI

Rabaneda-Bueno R., Aguado S., Fernández-Montraveta C., Moya-Laraño J. Does female personality determine mate choice through sexual cannibalism? Ethology. 2014;120 doi: 10.1111/eth.12197. DOI

Riechert S., Hedrick A. A test for correlations among fitness-linked behavioural traits in the spider Agelenopsis aperta (Araneae, Agelenidae) Anim. Behav. 1993;46:669–675. doi: 10.1006/anbe.1993.1243. DOI

Kralj-Fišer S., Čandek K., Lokovšek T., Čelik T., Cheng R.-C., Elgar M., Kuntner M. Mate choice and sexual size dimorphism, not personality, explain female aggression and sexual cannibalism in raft spiders. Anim. Behav. 2016;111 doi: 10.1016/j.anbehav.2015.10.013. DOI

Newman J., Elgar M. Sexual Cannibalism in Orb-Weaving Spiders: An Economic Model. Am. Nat. 1991;138:1372–1395. doi: 10.1086/285292. DOI

Moya-Laraño J., Orta-Ocaña J., José Antonio B., Bach C., Wise D. Intriguing compensation by adult female spiders for food limitation experienced as juveniles. Oikos. 2003;101:539–548. doi: 10.1034/j.1600-0706.2003.12316.x. DOI

Barry K., Holwell G., Herberstein M. Female praying mantids use sexual cannibalism as a foraging strategy to increase fecundity. Behav. Ecol. 2008;19:710–715. doi: 10.1093/beheco/arm156. DOI

Gavín Centol P., Kralj-Fišer S., De Mas Castroverde E., Ruiz-Lupión D., Moya-Laraño J. Feeding regime, adult age and sexual size dimorphism as determinants of pre-copulatory sexual cannibalism in virgin wolf spiders. Behav. Ecol. Sociobiol. 2017;71 doi: 10.1007/s00265-016-2228-6. DOI

Wilder S., Rypstra A. Sexual size dimorphism mediates the occurrence of state-dependent sexual cannibalism in a wolf spider. Anim. Behav. 2008;76:447–454. doi: 10.1016/j.anbehav.2007.12.023. DOI

Rabaneda-Bueno R., Rodríguez-Gironés M., Aguado S., Fernández-Montraveta C., De Mas Castroverde E., Wise D., Moya-Laraño J. Sexual Cannibalism: High Incidence in a Natural Population with Benefits to Females. PLoS ONE. 2008;3:e3484. doi: 10.1371/journal.pone.0003484. PubMed DOI PMC

Johnson J. Sexual cannibalism in fishing spiders (Dolomedes triton): An evaluation of two explanations for female aggression towards potential mates. Anim. Behav. 2001;61:905–914. doi: 10.1006/anbe.2000.1679. DOI

Erez T., Schneider J.M., Lubin Y. Is Male Cohabitation Costly for Females of the Spider Stegodyphus lineatus (Eresidae)? Ethology. 2005;111:693–704. doi: 10.1111/j.1439-0310.2005.01090.x. DOI

Dingemanse N., Both C., Drent P., Tinbergen J. Fitness consequences of avian personalities in a fluctuating environment. Proc. Biol. Sci. 2004;271:847–852. doi: 10.1098/rspb.2004.2680. PubMed DOI PMC

Dingemanse N., Réale D. Natural selection and animal personality. Behaviour. 2005;142 doi: 10.1163/156853905774539445. DOI

Smith B., Blumstein D. Fitness consequences of personality: A meta-analysis. Behav. Ecol. 2008;19:448–455. doi: 10.1093/beheco/arm144. DOI

Moya-Laraño J. Senescence and food limitation in a slowly aging spider. Funct. Ecol. 2002;16:734–741. doi: 10.1046/j.1365-2435.2002.00685.x. DOI

Moya-Laraño J., Orta-Ocana J., José Antonio B., Bach C., Wise D. Territoriality in a Cannibalistic Burrowing Wolf Spider. Ecology. 2002;83:356–361. doi: 10.2307/2680019. DOI

Biro P., Abrahams M., Post J., Parkinson E. Behavioural trade offs between growth and mortality explain evolution of submaximal growth rates. J. Anim. Ecol. 2006;75:1165–1171. doi: 10.1111/j.1365-2656.2006.01137.x. PubMed DOI

DeAngelis D.L., Mooij W.M. Individual-Based Modeling of Ecological and Evolutionary Processes. Annu. Rev. Ecol. Evol. Syst. 2005;36:147–168. doi: 10.1146/annurev.ecolsys.36.102003.152644. DOI

Deangelis D., Grimm V. Individual-based models in ecology after four decades. F1000Prime Rep. 2014;6:39. doi: 10.12703/P6-39. PubMed DOI PMC

Grimm V., Berger U., Bastiansen F., Eliassen S., Ginot V., Giske J., Goss-Custard J., Grand T., Heinz S., Huse G., et al. A Standard Protocol for Describing Individual-Based and Agent Based Models. Ecol. Modell. 2006;198:115–126. doi: 10.1016/j.ecolmodel.2006.04.023. DOI

Planas E., Fernández-Montraveta C., Ribera C. Molecular systematics of the wolf spider genus Lycosa (Araneae: Lycosidae) in the Western Mediterranean Basin. Mol. Phylogenet. Evol. 2013;67 doi: 10.1016/j.ympev.2013.02.006. PubMed DOI

Riechert S., Maynard-Smith J. Genetic analyses of two behavioural traits linked to individual fitness in the desert spider Agelenopsis aperta. Anim. Behav. 1989;37:624–637. doi: 10.1016/0003-3472(89)90041-9. DOI

Král J., Musilová J., Stahlavsky F., Rezác M., Akan Z., Edwards R., Coyle F., Ribera C. Evolution of the karyotype and sex chromosome systems in basal clades of araneomorph spiders (Araneae: Araneomorphae) Chromosome Res. 2006;14:859–880. doi: 10.1007/s10577-006-1095-9. PubMed DOI

Fernandez-Montraveta C., Ortega J. Sex differences in the agonistic behaviour of a lycosid spider (Araneae Lycosidae) Ethol. Ecol. Evol. 1993;5:293–301. doi: 10.1080/08927014.1993.9523017. DOI

Elgar M. Sperm Competition and Sexual Selection. Academic Press; Cambridge, MA, USA: 1998. Sperm Competition and Sexual Selection in Spiders and Other Arachnids; pp. 307–339.

Orta J.M., Moya-Laraño J., Barrientos J.A. Datos fenológicos de una población de Lycosa tarantula fasciiventris L. Dufour, 1835, en el Noroeste de la Península Ibérica (Araneae, Lycosidae) Bolletino Accad. Gioenia Sci. Nat. 1993;26:15–26.

Uhl G., Gunnarsson B. Female genitalia in Pityohyphantes phrygianus, a spider with a skewed sex ratio. J. Zool. 2001;255:367–376. doi: 10.1017/S0952836901001467. DOI

Jakob E., Marshall S., Uetz G., Jakob E.M., Marshall S.D., Uetz G.W. Estimating fitness: A comparison of body condition indices. Oikos. 1996;77:61. doi: 10.2307/3545585. DOI

Moya-Laraño J., Pascual J., Wise D. Approach Strategy by which Male Mediterranean Tarantulas Adjust to the Cannibalistic Behaviour of Females. Ethology. 2004;110:717–724. doi: 10.1111/j.1439-0310.2004.01012.x. DOI

Moya-Laraño J. Ph.D. Thesis. Universitat Autònoma de Barcelona; Barcelona, Spain: 1999. Limitación por el Alimento, Territorialidad y Canibalismo en la Tarántula Mediterránea, Lycosa tarentula (L.) (Araneae, Lycosidae)

Moya-Laraño J., Macías-Ordóñez R., Blanckenhorn W., Fernández-Montraveta C. Analysing body condition: Mass, volume or density? J. Anim. Ecol. 2008;77:1099–1108. doi: 10.1111/j.1365-2656.2008.01433.x. PubMed DOI

Higgins E., Rankin A. Mortality risk of rapid growth in the spider Nephila clavipes. Funct. Ecol. 2001;15:24–28. doi: 10.1046/j.1365-2435.2001.00491.x. DOI

Uetz G. Foraging strategies of spiders. Trends Ecol. Evol. 1992;7:155–159. doi: 10.1016/0169-5347(92)90209-T. PubMed DOI

Prokop P., Václav R. Seasonal aspects of sexual cannibalism in the praying mantis (Mantis religiosa) J. Ethol. 2008;26:213–218. doi: 10.1007/s10164-007-0050-3. DOI

Samu F., Toft S., Kiss B., Samu F., Toft S., Kiss B. Factors influencing cannibalism in the wolf spider Pardosa agrestis (Araneae, Lycosidae) Behav. Ecol. Sociobiol. 1999;45:349–354. doi: 10.1007/s002650050570. DOI

Wise D. Spiders in Ecological Webs. Cambridge University Press; Cambridge, UK: 1993. DOI

Rabaneda-Bueno R. Ph.D. Thesis. Autonomous University of Madrid; Madrid, Spain: 2014. El Canibalismo Sexual en la Tarántula Ibérica (Lycosa hispanica): Ecología y Evolución de Estrategias Conductuales.

R Core Development Team . R: A Language and Environment for Statistical Computing. R Core; Vienna, Austria: 2014.

Luttbeg B., Sih A. Risk, resources and state-dependent adaptive behavioural syndromes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2010;365:3977–3990. doi: 10.1098/rstb.2010.0207. PubMed DOI PMC

Moya-Laraño J., Verdeny-Vilalta O., Rowntree J., Melguizo-Ruiz N., Montserrat M., Laiolo P. Climate Change and Eco-Evolutionary Dynamics in Food Webs. Adv. Ecol. Res. 2012;47:1–80. doi: 10.1016/B978-0-12-398315-2.00001-6. DOI

Morse D. A test of sexual cannibalism models, using a sit-and-wait predator. Biol. J. Linn. Soc. 2004;81:427–437. doi: 10.1111/j.1095-8312.2003.00294.x. DOI

Morse D. Mating frequencies of male crab spiders, Misumena vatia (Araneae, Thomisidae) J. Arachnol. 2007;35:84–88. doi: 10.1636/ST06-13.1. DOI

Legrand R., Morse D. Factors driving extreme sexual size dimorphism of a sit-and-wait predator under low density. Biol. J. Linn. Soc. 2008;71:643–664. doi: 10.1111/j.1095-8312.2000.tb01283.x. DOI

Darwin C. The Descent of Man and Selection in Relation to Sex. 1st ed. John Murray; London, UK: 1871. DOI

Kreiter N., Wise D. Age-related changes in movement patterns in the fishing spider, Dolomedes triton (Araneae, Pisauridae) J. Arachnol. 1996;24:24–33.

Kreiter N., Wise D. Prey availability limits fecundity and movement patterns of female fishing spiders. Oecologia. 2001;127:417–424. doi: 10.1007/s004420000607. PubMed DOI

Aisenberg A., Viera C., Costa F.G. Daring females, devoted males, and reversed sexual size dimorphism in the sand-dwelling spider Allocosa brasiliensis (Araneae, Lycosidae) Behav. Ecol. Sociobiol. 2007;62:29–35. doi: 10.1007/s00265-007-0435-x. DOI

Foellmer M., Moya-Laraño J. Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism. Oxford University Press; New York, NY, USA: 2007. Sexual size dimorphism in spiders: Patterns and processes; pp. 71–81.

Hurd L., Eisenberg R., Fagan W., Tilmon K., Snyder W., Vandersall K., Datz S., Welch J. Cannibalism Reverses Male-Biased Sex Ratio in Adult Mantids: Female Strategy against Food Limitation? Oikos. 1994;69:193. doi: 10.2307/3546137. DOI

Fitzpatrick M., Feder E., Rowe L., Sokolowski M. Maintaining a behavior polymorphism by frequency-dependent selection on a single gene. Nature. 2007;447:210–212. doi: 10.1038/nature05764. PubMed DOI

Wright S. On the roles of directed and random changes in gene frequency in the genetics of populations. Evolution. 1948;2:279–294. doi: 10.1111/j.1558-5646.1948.tb02746.x. PubMed DOI

Fisher R.A. The Genetic Theory of Natural Selection. Oxford University Press; Oxford, UK: 1930.

Clarke B., O’Donald P. Frequency-dependent selection. Heredity (Edinb.) 1964;19:201–206. doi: 10.1038/hdy.1964.25. DOI

Wolf M., van Doorn S., Leimar O., Weissing F. Life history tradeoffs favour the evolution of personality. Nature. 2007;447:581–584. doi: 10.1038/nature05835. PubMed DOI

Neff B., Sherman P. Behavioral syndromes versus Darwinian algorithms. Trends Ecol. Evol. 2004;19 doi: 10.1016/j.tree.2004.09.017. DOI

Ruiz-Gomez M.D.L., Kittilsen S., Höglund E., Huntingford F., Sørensen C., Pottinger T., Bakken M., Winberg S., Korzan W., Øverli Ø. Behavioral plasticity in rainbow trout (Oncorhynchus mykiss) with divergent coping styles: When doves become hawks. Horm. Behav. 2008;54:534–538. doi: 10.1016/j.yhbeh.2008.05.005. PubMed DOI

Brodin T. Behavioral syndrome over the boundaries of life-025EFcarryovers from larvae to adult damselfly. Behav. Ecol. 2009;20:30–37. doi: 10.1093/beheco/arn111. DOI

Minderman J., Reid J., Evans P., Whittingham M. Personality traits in wild starlings: Exploration behavior and environmental sensitivity. Behav. Ecol. 2009;20:830–837. doi: 10.1093/beheco/arp067. DOI

Nelson X., Wilson D., Evans C. Behavioral Syndromes in Stable Social Groups: An Artifact of External Constraints? Ethology. 2008;114:1154–1165. doi: 10.1111/j.1439-0310.2008.01568.x. DOI

Wilson A., Godin J.-G. Boldness and behavioral syndromes in the bluegill sunfish, Lepomis macrochirus. Behav. Ecol. 2009;20:231–237. doi: 10.1093/beheco/arp018. DOI

Logue D., Mishra S., McCaffrey D., Ball D., Cade W. A behavioral syndrome linking courtship behavior toward males and females predicts reproductive success from a single mating in the hissing cockroach, Gromphadorhina portentosa. Behav. Ecol. 2009;20:781–788. doi: 10.1093/beheco/arp061. DOI

Gould S.J. Only his wings remained. Nat. Hist. 1984;93:10–18.

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