The evolution of age-specific choosiness and reproductive isolation in a model with overlapping generations.
Age
choosiness
life history
reproductive isolation
speciation
Journal
Evolution; international journal of organic evolution
ISSN: 1558-5646
Titre abrégé: Evolution
Pays: United States
ID NLM: 0373224
Informations de publication
Date de publication:
02 2022
02 2022
Historique:
received:
22
10
2020
accepted:
31
10
2021
pubmed:
9
12
2021
medline:
5
3
2022
entrez:
8
12
2021
Statut:
ppublish
Résumé
The strength of mate choice (choosiness) often varies with age, but theory to understand this variation is scarce. Additionally, theory has investigated the evolution of choosiness in speciation scenarios but has ignored that most organisms have overlapping generations. We investigate whether speciation can result in variation of choosiness with age, and whether such variation can in turn affect speciation. We develop a population-genetic model of the evolution of choosiness in organisms with overlapping generations in the context of secondary contact between two divergent populations. We assume that females choose males that match their phenotype, such that choosiness evolves by sexual selection. We demonstrate that speciation can result in the evolution of age-specific choosiness when the mating trait is under divergent ecological selection and age is not used as a mating cue. The cause of this result is that allele frequencies differ between choosy females and males. However, we find that the evolution of age-specific choosiness does not affect the overall level of reproductive isolation compared to a case without age-structure, supporting previous speciation theory. Overall, our results connect life history and speciation theory, and the mechanisms that we highlight have implications for the understanding of the role of sex-specific selection in the evolution of choosiness.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
225-235Informations de copyright
© 2021 The Authors. Evolution © 2021 The Society for the Study of Evolution.
Références
Alatalo, R. V., D. Eriksson, L. Gustafsson, and A. Lundberg. 1990. Hybridization between pied and collared flycatchers-sexual selection and speciation theory. J. Evol. Biol. 3:375-389.
Barton, N., and M. Turelli. 1991. Natural and sexual selection on many loci. Genet. 127:229-255.
Baugh, A. T., and M. J. Ryan. 2010. The development of sexual behavior in tungara frogs (physalaemus pustulosus). J. Comp. Psychol. 124:66.
Beck, C. W., B. Shapiro, S. Choksi, and D. E. Promislow. 2002. A genetic algorithm approach to study the evolution of female preference based on male age. Evol. Ecol. Res. 4:275-292.
Bonduriansky, R., A. Maklakov, F. Zajitschek, and R. Brooks. 2008. Sexual selection, sexual conflict and the evolution of ageing and life span. Funct. Ecol. 22:443-453.
Bouwhuis, S., B. Sheldon, S. Verhulst, and A. Charmantier. 2009. Great tits growing old: selective disappearance and the partitioning of senescence to stages within the breeding cycle. Proc. Roy. Soc. B: Biol. Sci. 276:2769-2777.
Cheng, C., and M. Kirkpatrick. 2016. Sex-specific selection and sex-biased gene expression in humans and flies. PLoS Genet. 12:e1006170.
Cotto, O., and T. Day. 2021. The evolution of age-specific choosiness when mating. J. Evol. Biol. 34:477-485.
Cotto, O., and M. R. Servedio. 2017. The roles of sexual and viability selection in the evolution of incomplete reproductive isolation: from allopatry to sympatry. Am. Nat. 190:680-693.
Etienne, L., F. Rousset, B. Godelle, and A. Courtiol. 2014. How choosy should i be? the relative searching time predicts evolution of choosiness under direct sexual selection. Proc. Roy. Soc. B: Biol. Sci. 281:20140190.
Gavrilets, S. 2004. Fitness landscapes and the origin of species (MPB-41), vol. 41. Princeton Univ. Press, Princeton, NJ.
Geritz, S. A., G. Mesze, J. A. Metz, et al. 1998. Evolutionarily singular strategies and the adaptive growth and branching of the evolutionary tree. Evol. Ecol. 12:35-57.
Gilman, R. T., K. Fowler-Finn, and E. A. Hebets. 2018. A probable case of incipient speciation in schizocosa wolf spiders driven by allochrony, habitat use, and female mate choice. Amer. Nat. 192:332-346.
A Gray, D. 1999. Intrinsic factors affecting female choice in house crickets: time cost, female age, nutritional condition, body size, and size-relative reproductive investment. J. Insect Behav. 12:691-700.
Hassall, C., T. N. Sherratt, P. C. Watts, and D. J. Thompson. 2015. Live fast, die old: no evidence of reproductive senescence or costs of mating in a damselfly (odonata: Zygoptera). J. Anim. Ecol. 84:1542-1554.
M Henshaw, J. 2018. Finding the one: optimal choosiness under sequential mate choice. J. Evol. Biol. 31:1193-1203.
C Janetos, A. 1980. Strategies of female mate choice: a theoretical analysis. Behav. Ecol. Sociobiol. 7:107-112.
Janicke, T., L. Marie-Orleach, T. G. Aubier, C. Perrier, and E. H. Morrow. 2019. Assortative mating in animals and its role for speciation. Amer. Nat. 194:865-875.
Jennions, M. D., and M. Petrie. 1997. Variation in mate choice and mating preferences: a review of causes and consequences. Biol. Rev. 72:283-327.
Jiang, Y., D. I. Bolnick, and M. Kirkpatrick. 2013. Assortative mating in animals. Am. Nat. 181:E125-E138.
Jiggins, C. D., R. E. Naisbit, R. L. Coe, and J. Mallet. 2001. Reproductive isolation caused by colour pattern mimicry. Nature 411:302-305.
Jouventin, P., B. Lequette, and F. S. Dobson. 1999. Age-related mate choice in the wandering albatross. Anim. Behav. 57:1099-1106.
Kodric-Brown, A., and P. F. Nicoletto. 2001. Age and experience affect female choice in the guppy (poecilia reticulata). Am. Nat. 157:316-323.
Kokko, H. 1998. Good genes, old age and life-history trade-offs. Evol. Ecol. 12:739-750.
Kokko, H., and J. Lindström. 1996. Evolution of female preference for old mates. Proc. Roy. Soc. Lond. Ser. B: Biol. Sci. 263:1533-1538.
Kopp, M., M. R. Servedio, T. C. Mendelson, R. J. Safran, R. L. Rodríguez, M. E. Hauber, E. C. Scordato, L. B. Symes, C. N. Balakrishnan, D. M. Zonana, et al. 2018. Mechanisms of assortative mating in speciation with gene flow: connecting theory and empirical research. Am. Nat. 191:1-20.
Kronforst, M. R., L. G. Young, D. D. Kapan, C. McNeely, R. J. O'Neill, and L. E. Gilbert. 2006. Linkage of butterfly mate preference and wing color preference cue at the genomic location of wingless. Proc. Nat. Acad. Sci. U.S.A. 103:6575-6580.
Moore, P. J., and A. J. Moore. 2001. Reproductive aging and mating: the ticking of the biological clock in female cockroaches. Proc. Nat. Acad. Sci. U.S.A. 98:9171-9176.
Moran, P. 1959. The theory of some genetical effects of population subdivision. Aust. J. Biol. Sci. 12:109-116.
Nosil, P., B. Crespi, and C. Sandoval. 2003. Reproductive isolation driven by the combined effects of ecological adaptation and reinforcement. Proc. Roy. Soc. London. Ser. B: Biol. Sci. 270:1911-1918.
Priklopil, T., E. Kisdi, and M. Gyllenberg. 2015. Evolutionarily stable mating decisions for sequentially searching females and the stability of reproductive isolation by assortative mating. Evol. 69:1015-1026.
Proulx, S. R., T. Day, and L. Rowe. 2002. Older males signal more reliably. Proc. Roy. Soc. Lond. Ser. B: Biol. Sci. 269:2291-2299.
Ronald, K. L., E. Fernández-Juricic, and J. R. Lucas. 2012. Taking the sensory approach: how individual differences in sensory perception can influence mate choice. Anim. Behav. 84:1283-1294.
Rosenthal, G. G. 2017. Mate choice: the evolution of sexual decision making from microbes to humans. Princeton Univ. Press, Princeton, NJ.
R Servedio, M. 2011. Limits to the evolution of assortative mating by female choice under restricted gene flow. Proc. R. Soc. B: Biol. Sci. 278:179-187.
Servedio, M. R., and J. W. Boughman. 2017. The role of sexual selection in local adaptation and speciation. Annu. Rev. Ecol. Evol. Systematics. 48:85-109.
Servedio, M. R., and R. Bürger. 2020. The effectiveness of pseudomagic traits in promoting divergence and enhancing local adaptation. Evol.
Servedio, M. R., and J. Hermisson. 2020. The evolution of partial reproductive isolation as an adaptive optimum. Evolution 74:4-14.
Servedio, M. R., G. S. Van Doorn, M. Kopp, A. M. Frame, and P. Nosil. 2011. Magic traits in speciation: ‘magic’ but not rare? Trends Ecol. Evol. 26:389-397.
Sozou, P. D., and R. M. Seymour. 2003. Augmented discounting: interaction between ageing and time-preference behaviour. Proc. Roy. Soc. London. Ser. B: Biol. Sci. 270(1519): 1047-1053.
Summers, K., R. Symula, M. Clough, and T. Cronin. 1999. Visual mate choice in poison frogs. Proc. Roy. Soc. Lond. Ser. B: Biol. Sci. 266:2141-2145.
Vaupel, J. W., K. G. Manton, and E. Stallard. 1979. The impact of heterogeneity in individual frailty on the dynamics of mortality. Demography 16:439-454.