Disentangling the causes of temporal variation in the opportunity for sexual selection
Darwin, C. The Descent of Man and Selection in Relation to Sex. (John Murray, 1871).Andersson, M. Sexual Selection. (Princeton University Press, 1994).Shuster, S. & Wade, M. J. Mating Systems and Strategies. (Princeton University Press, 2003).Gosden, T. P. & Svensson, E. I. Spatial and temporal dynamics in a sexual selection mosaic. Evolution 62, 845–856 (2008).Article
PubMed
Google Scholar
Kasumovic, M. M., Bruce, M. J., Andrade, M. C. B. & Herberstein, M. E. Spatial and temporal demographic variation drives within-season fluctuations in sexual selection. Evolution 62, 2316–2325 (2008).Article
PubMed
Google Scholar
Mobley, K. B. & Jones, A. G. Environmental, demographic, and genetic mating system variation among five geographically distinct dusky pipefish (Syngnathus floridae) populations. Mol. Ecol. 18, 1476–1490 (2009).Article
PubMed
Google Scholar
Hoffer, J. N., Mariën, J., Ellers, J. & Koene, J. M. Sexual selection gradients change over time in a simultaneous hermaphrodite. eLife 6, e25139 (2017).Article
PubMed
PubMed Central
Google Scholar
Sih, A., Montiglio, P.-O., Wey, T. W. & Fogarty, S. Altered physical and social conditions produce rapidly reversible mating systems in water striders. Behav. Ecol. 28, 632–639 (2017).Article
Google Scholar
Preston, B. T., Stevenson, I. R., Pemberton, J. M. & Wilson, K. Dominant rams lose out by sperm depletion. Nature 409, 681–682 (2001).Article
ADS
CAS
PubMed
Google Scholar
Cornwallis, C. K. & Uller, T. Towards an evolutionary ecology of sexual traits. Trends Ecol. Evol. 25, 145–152 (2010).Article
PubMed
Google Scholar
Forsgren, E., Amundsen, T., Borg, A. A. & Bjelvenmark, J. Unusually dynamic sex roles in a fish. Nature 429, 551–554 (2004).Article
ADS
CAS
PubMed
Google Scholar
Hare, R. M. & Simmons, L. W. Sexual selection maintains a female-specific character in a species with dynamic sex roles. Behav. Ecol. 32, 609–616 (2021).Article
Google Scholar
Fox, R. J., Donelson, J. M., Schunter, C., Ravasi, T. & Gaitán-Espitia, J. D. Beyond buying time: the role of plasticity in phenotypic adaptation to rapid environmental change. Philos. Trans. R. Soc. B 374, 20180174 (2019).Article
Google Scholar
Ingleby, F. C., Hunt, J. & Hosken, D. J. The role of genotype-by-environment interactions in sexual selection. J. Evol. Biol. 23, 2031–2045 (2010).Article
CAS
PubMed
Google Scholar
Lindström, J., Pike, T. W., Blount, J. D. & Metcalfe, N. B. Optimization of resource allocation can explain the temporal dynamics and honesty of sexual signals. Am. Nat. 174, 515–525 (2009).Article
PubMed
Google Scholar
Janicke, T., David, P. & Chapuis, E. Environment-dependent sexual selection: Bateman’s parameters under varying levels of food availability. Am. Nat. 185, 756–768 (2015).Article
PubMed
Google Scholar
Morimoto, J., Pizzari, T. & Wigby, S. Developmental environment effects on sexual selection in male and female Drosophila melanogaster. PLoS ONE 11, e0154468 (2016).Article
PubMed
PubMed Central
Google Scholar
Cattelan, S., Evans, J. P., Garcia-Gonzalez, F., Morbiato, E. & Pilastro, A. Dietary stress increases the total opportunity for sexual selection and modifies selection on condition-dependent traits. Ecol. Lett. 23, 447–456 (2020).Article
PubMed
Google Scholar
Glavaschi, A., Cattelan, S., Grapputo, A. & Pilastro, A. Imminent risk of predation reduces the relative strength of postcopulatory sexual selection in the guppy. Philos. Trans. R. Soc. B 375, 20200076 (2020).Article
Google Scholar
Clark, D. C., DeBano, S. J. & Moore, A. J. The influence of environmental quality on sexual selection in Nauphoeta cinerea (Dictyoptera: Blaberidae). Behav. Ecol. 8, 46–53 (1997).Article
Google Scholar
Emlen, S. & Oring, L. Ecology, sexual selection and the evolution of mating systems. Science 197, 215–223 (1977).Article
ADS
CAS
PubMed
Google Scholar
Liker, A., Freckleton, R. P. & Székely, T. The evolution of sex roles in birds is related to adult sex ratio. Nat. Commun. 4, 1–6 (2013).Article
Google Scholar
Wacker, S. et al. Operational sex ratio but not density affects sexual selection in a fish. Evolution 67, 1937–1949 (2013).Article
PubMed
Google Scholar
Wacker, S., Ness, M. H., Östlund-Nilsson, S. & Amundsen, T. Social structure affects mating competition in a damselfish. Coral Reefs 36, 1279–1289 (2017).Article
ADS
Google Scholar
Janicke, T. & Morrow, E. H. Operational sex ratio predicts the opportunity and direction of sexual selection across animals. Ecol. Lett. 21, 384–391 (2018).Article
PubMed
Google Scholar
Procter, D. S., Moore, A. J. & Miller, C. W. The form of sexual selection arising from male-male competition depends on the presence of females in the social environment. J. Evol. Biol. 25, 803–812 (2012).Article
CAS
PubMed
Google Scholar
Eldakar, O. T., Dlugos, M. J., Pepper, J. W. & Wilson, D. S. Population structure mediates sexual conflict in Water striders. Science 326, 816–816 (2009).Article
ADS
CAS
PubMed
Google Scholar
Martin, A. M., Festa-Bianchet, M., Coltman, D. W. & Pelletier, F. Demographic drivers of age-dependent sexual selection. J. Evol. Biol. 29, 1437–1446 (2016).Article
CAS
PubMed
Google Scholar
Pilakouta, N. & Ålund, M. Sexual selection and environmental change: what do we know and what comes next? Curr. Zool. 67, 293–298 (2021).Article
PubMed
PubMed Central
Google Scholar
Kahn, A. T., Dolstra, T., Jennions, M. D. & Backwell, P. R. Y. Strategic male courtship effort varies in concert with adaptive shifts in female mating preferences. Behav. Ecol. 24, 906–913 (2013).Article
Google Scholar
Jordan, L. A. & Brooks, R. C. Recent social history alters male courtship preferences. Evolution 66, 280–287 (2012).Article
PubMed
Google Scholar
Wilson, D. R., Nelson, X. J. & Evans, C. S. Seizing the opportunity: Subordinate male fowl respond rapidly to variation in social context. Ethology 115, 996–1004 (2009).Article
Google Scholar
Gwynne, D. T., Bailey, W. J. & Annells, A. The sex in short supply for matings varies over small Spatial scales in a Katydid (Kawanaphila nartee, Orthoptera: Tettigoniidae). Behav. Ecol. Sociobiol. 42, 157–162 (1998).Article
Google Scholar
Fedina, T. Y. & Lewis, S. M. Female mate choice across mating stages and between sequential mates in flour beetles. J. Evol. Biol. 20, 2138–2143 (2007).Article
CAS
PubMed
Google Scholar
Clark, H. L. & Backwell, P. R. Y. Temporal and spatial variation in female mating preferences in a fiddler crab. Behav. Ecol. Sociobiol. 69, 1779–1784 (2015).Article
Google Scholar
Serbezov, D., Bernatchez, L., Olsen, E. M. & Vøllestad, L. A. Mating patterns and determinants of individual reproductive success in brown trout (Salmo trutta) revealed by parentage analysis of an entire stream living population. Mol. Ecol. 19, 3193–3205 (2010).Article
PubMed
Google Scholar
Gerlach, N. M., McGlothlin, J. W., Parker, P. G. & Ketterson, E. D. Reinterpreting Bateman gradients: multiple mating and selection in both sexes of a songbird species. Behav. Ecol. 23, 1078–1088 (2012).Article
Google Scholar
Dubuc, C., Ruiz-Lambides, A. & Widdig, A. Variance in male lifetime reproductive success and estimation of the degree of polygyny in a primate. Behav. Ecol. 25, 878–889 (2014).Article
PubMed
PubMed Central
Google Scholar
Breuer, T. et al. Variance in the male reproductive success of western gorillas: acquiring females is just the beginning. Behav. Ecol. Sociobiol. 64, 515–528 (2010).Article
Google Scholar
Germain, R. R., Hallworth, M. T., Kaiser, S. A., Sillett, T. S. & Webster, M. S. Variance in within-pair reproductive success influences the opportunity for selection annually and over the lifetimes of males in a multi-brooded songbird. Evolution 75, 915–930 (2021).Article
PubMed
Google Scholar
Lande, R. & Arnold, S. J. The measurement of selection on correlated characters. Evolution 37, 1210–1226 (1983).Article
PubMed
Google Scholar
Klug, H., Heuschele, J., Jennions, M. D. & Kokko, H. The mismeasurement of sexual selection. J. Evol. Biol. 23, 447–462 (2010).Article
CAS
PubMed
Google Scholar
Jennions, M. D., Kokko, H. & Klug, H. The opportunity to be misled in studies of sexual selection. J. Evol. Biol. 25, 591–598 (2012).Article
CAS
PubMed
Google Scholar
Krakauer, A. H., Webster, M. S., Duval, E. H., Jones, A. G. & Shuster, S. M. The opportunity for sexual selection: not mismeasured, just misunderstood. J. Evol. Biol. 24, 2064–2071 (2011).Article
CAS
PubMed
Google Scholar
Hebets, E. A., Stafstrom, J. A., Rodriguez, R. L. & Wilgers, D. J. Enigmatic ornamentation eases male reliance on courtship performance for mating success. Anim. Behav. 81, 963–972 (2011).Article
Google Scholar
Fitzpatrick, J. L. & Lüpold, S. Sexual selection and the evolution of sperm quality. Mol. Hum. Reprod. 20, 1180–1189 (2014).Article
PubMed
Google Scholar
Jones, A. G. On the opportunity for sexual selection, the Bateman gradient and the maximum intensity of sexual selection. Evolution 63, 1673–1684 (2009).Article
PubMed
Google Scholar
Henshaw, J. M., Kahn, A. T. & Fritzsche, K. A rigorous comparison of sexual selection indexes via simulations of diverse mating systems. Proc. Natl Acad. Sci. USA 113, E300–E308 (2016).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Evans, J. P. & Garcia-Gonzalez, F. The total opportunity for sexual selection and the integration of pre- and post-mating episodes of sexual selection in a complex world. J. Evol. Biol. 29, 2338–2361 (2016).Article
CAS
PubMed
Google Scholar
Downhower, J. F., Blumer, L. S. & Brown, L. Opportunity for selection: an appropriate measure for evaluating variation in the potential for selection? Evolution 41, 1395–1400 (1987).Article
PubMed
Google Scholar
Klug, H. & Stone, L. More than just noise: Chance, mating success, and sexual selection. Ecol. Evol. 11, 6326–6340 (2021).Article
PubMed
PubMed Central
Google Scholar
Anthes, N., Häderer, I. K., Michiels, N. K. & Janicke, T. Measuring and interpreting sexual selection metrics: evaluation and guidelines. Methods Ecol. Evol. 8, 918–931 (2016).Article
Google Scholar
Klug, H., Lindström, K. & Kokko, H. Who to include in measures of sexual selection is no trivial matter. Ecol. Lett. 13, 1094–1102 (2010).Article
PubMed
Google Scholar
Collet, J. M., Dean, R. F., Worley, K., Richardson, D. S. & Pizzari, T. The measure and significance of Bateman’s principles. Proc. R. Soc. B 281, 20132973 (2014).Article
PubMed
PubMed Central
Google Scholar
Collet, J., Richardson, D. S., Worley, K. & Pizzari, T. Sexual selection and the differential effect of polyandry. Proc. Natl Acad. Sci. USA 109, 8641–8645 (2012).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
McDonald, G. C., Spurgin, L. G., Fairfield, E. A., Richardson, D. S. & Pizzari, T. Pre- and postcopulatory sexual selection favor aggressive, young males in polyandrous groups of red junglefowl. Evolution 71, 1653–1669 (2017).Article
PubMed
Google Scholar
Morimoto, J. et al. Sex peptide receptor-regulated polyandry modulates the balance of pre- and post-copulatory sexual selection in Drosophila. Nat. Commun. 10, 283 (2019).Article
ADS
PubMed
PubMed Central
Google Scholar
Shuster, S. M., Willen, R. M., Keane, B. & Solomon, N. G. Alternative mating tactics in socially monogamous prairie voles, Microtus ochrogaster. Front. Ecol. Evol. 7, 7 (2019).Article
Google Scholar
Dowling, J. & Webster, M. S. Working with what you’ve got: unattractive males show greater mate-guarding effort in a duetting songbird. Biol. Lett. 13, 20160682 (2017).Article
PubMed
PubMed Central
Google Scholar
Pizzari, T. & McDonald, G. C. Sexual selection in socially structured, polyandrous populations: Some insights from the fowl. Adv. Study Behav. 51, 77–141 (2019).Article
Google Scholar
Archer, M. S. & Elgar, M. A. Female preference for multiple partners: sperm competition in the hide beetle, Dermestes maculatus (DeGeer). Anim. Behav. 58, 669–675 (1999).Article
CAS
PubMed
Google Scholar
Qvarnström, A. & Forsgren, E. Should females prefer dominant males? Trends Ecol. Evol. 13, 498–501 (1998).Article
PubMed
Google Scholar
Webster, M. S., Tarvin, K. A., Tuttle, E. M. & Pruett-Jones, S. Promiscuity drives sexual selection in a socially monogamous bird. Evolution 61, 2205–2211 (2007).Article
PubMed
Google Scholar
Brunton, D. H. Energy expenditure in reproductive effort of male and female Killdeer (Charadrius vociferus). Auk 105, 553–564 (1988).Article
Google Scholar
Johnson, L. S., Hicks, B. G. & Masters, B. S. Increased cuckoldry as a cost of breeding late for male house wrens (Troglodytes aedon). Behav. Ecol. 13, 670–675 (2002).Article
Google Scholar
Boinski, S. Mating patterns in squirrel monkeys (Saimiri oerstedi): implications for seasonal sexual dimorphism. Behav. Ecol. Sociobiol. 21, 13–21 (1987).Article
Google Scholar
McDonald, G. C., Spurgin, L. G., Fairfield, E. A., Richardson, D. S. & Pizzari, T. Differential female sociality is linked with the fine-scale structure of sexual interactions in replicate groups of red junglefowl, Gallus gallus. Proc. R. Soc. B 286, 20191734 (2019).Article
PubMed
PubMed Central
Google Scholar
Carleial, R. et al. Temporal dynamics of competitive fertilization in social groups of red junglefowl (Gallus gallus) shed new light on avian sperm competition. Philos. Trans. R. Soc. B 375, 20200081 (2020).Article
Google Scholar
Lessells, C. M. & Birkhead, T. R. Mechanisms of sperm competition in birds: mathematical models. Behav. Ecol. Sociobiol. 27, 325–337 (1990).Article
Google Scholar
Taborsky, T., Oliveira, R. F. & Brockmann, H. J. The Evolution of Alternative Reproductive Tactics: Concepts and Questions. in Alternative Reproductive Tactics: An Integrative Approach (Cambridge University Press, 2008).Ghislandi, P. G. et al. Resource availability, mating opportunity and sexual selection intensity influence the expression of male alternative reproductive tactics. J. Evol. Biol. 31, 1035–1046 (2018).Article
PubMed
Google Scholar
Lehtonen, T. K., Wong, B. B. M. & Lindström, K. Fluctuating mate preferences in a marine fish. Biol. Lett. 6, 21–23 (2010).Article
PubMed
Google Scholar
Chaine, A. S. & Lyon, B. E. Adaptive plasticity in female mate choice dampens sexual selection on male ornaments in the lark bunting. Science 319, 459–462 (2008).Article
ADS
CAS
PubMed
Google Scholar
R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2019).Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting Linear Mixed-Effects Models Using lme4. J. Stat. Softw. 67, 1–48 (2015).Article
Google Scholar
Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. lmerTest package: tests in linear mixed effects models. J. Stat. Softw. 82, 1–26 (2017).Article
Google Scholar
Oklander, L. I., Kowalewski, M. & Corach, D. Male reproductive strategies in black and gold howler monkeys (Alouatta caraya). Am. J. Primatol. 76, 43–55 (2014).Article
PubMed
Google Scholar
Pröhl, H. & Hödl, W. Parental investment, potential reproductive rates, and mating system in the strawberry dart-poison frog, Dendrobates pumilio. Behav. Ecol. Sociobiol. 46, 215–220 (1999).Article
Google Scholar
Turnell, B. R. & Shaw, K. L. High opportunity for postcopulatory sexual selection under field conditions. Evolution 69, 2094–2104 (2015).Article
PubMed
Google Scholar
Gill, L. F., van Schaik, J., von Bayern, A. M. P. & Gahr, M. L. Genetic monogamy despite frequent extrapair copulations in “strictly monogamous” wild jackdaws. Behav. Ecol. 31, 247–260 (2020).Article
PubMed
Google Scholar
Carleial, R., McDonald, G. C. & Pizzari, T. Dynamic phenotypic correlates of social status and mating effort in male and female red junglefowl, Gallus gallus. J. Evol. Biol. 33, 22–40 (2020).Article
PubMed
Google Scholar
McDonald, G. C. & Pizzari, T. Structure of sexual networks determines the operation of sexual selection. Proc. Natl Acad. Sci. USA 115, E53–E61 (2018).Article
ADS
CAS
PubMed
Google Scholar
Janicke, T., Häderer, I. K., Lajeunesse, M. J. & Anthes, N. Darwinian sex roles confirmed across the animal kingdom. Sci. Adv. 2, e1500983 (2016).Article
ADS
PubMed
PubMed Central
Google Scholar
Webster, M. S., Pruett-Jones, S., Westneat, D. F. & Arnold, S. J. Measuring the effects of pairing success, extra-pair copulations and mate quality on the opportunity for sexual selection. Evolution 49, 1147–1157 (1995).PubMed
Google Scholar
Etches, R. J. Reproduction in Poultry. (CABI, 1996).Schielzeth, H. Simple means to improve the interpretability of regression coefficients: Interpretation of regression coefficients. Methods Ecol. Evol. 1, 103–113 (2010).Article
Google Scholar
Løvlie, H., Cornwallis, C. K. & Pizzari, T. Male mounting alone reduces female promiscuity in the fowl. Curr. Biol. 15, 1222–1227 (2005).Article
PubMed
Google Scholar
Berglund, A. Many mates make male pipefish choosy. Behaviour 132, 213–218 (1995).Article
Google Scholar
Carleial, R., Pizzari, T., Richardson, D. S. & McDonald, G. C. Data for: Disentangling the causes of temporal variation in the opportunity for sexual selection. figshare Dataset (2023) https://doi.org/10.6084/m9.figshare.21902133.v1.McLain, D. K., Burnette, L. B. & Deeds, D. A. Within season variation in the intensity of sexual selection on body size in the bug Margus obscurator (Hemiptera Coreidae). Ethol. Ecol. Evol. 5, 75–86 (1993).Article
Google Scholar
Schlicht, E. & Kempenaers, B. Effects of social and extra-pair mating on sexual selection in Blue tits (Cyanistes caeruleus). Evolution 67, 1420–1434 (2013).PubMed
Google Scholar More