Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Paternity analysis reveals sexual selection on cognitive performance in mosquitofish

Nature Ecology & Evolution volume 9, pages 692–704 (2025)Cite this article

Subjects

Abstract

In many animal species, cognitive abilities are under strong natural selection because decisions about foraging, habitat choice and predator avoidance affect fecundity and survival. But how has sexual selection, which is usually stronger on males than females, shaped the evolution of cognitive abilities that influence success when competing for mates or fertilizations? We aimed to investigate potential links between individual differences in male cognitive performance to variation in paternity arising solely from sexual selection. We therefore ran four standard cognitive assays to quantify five measures of cognitive performance by male mosquitofish (Gambusia holbrooki). Males were then assigned to 11 outdoor ponds where they could compete for females. Females mate many times, which leads to intense sperm competition and broods with mixed paternity. We genotyped 2,430 offspring to identify their fathers. Males with greater inhibitory control and better spatial learning abilities sired significantly more offspring, while males with better initial impulse control sired significantly fewer offspring. Associative and reversal learning did not predict a male’s share of paternity. In sum, there was sexual selection on several, but not all, aspects of male cognitive performance.

Access through your institution
Buy or subscribe

This is a preview of subscription content, access via your institution

Access options

Access through your institution

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Timeline of the study.
Fig. 2: Correlation matrix of cognitive scores.
Fig. 3: Spearman’s correlations between share of paternity and five cognitive traits, a CCS, boldness and body size of male G. holbrooki.

Similar content being viewed by others

Data availability

The data that support the findings of this study are available via figshare at https://figshare.com/s/4cc0aeaa01188668c0e7 (ref. 114).

Code availability

The R code is available via figshare at https://figshare.com/s/4cc0aeaa01188668c0e7 (ref. 114).

References

  1. Shettleworth, S. J. Cognition, Evolution, and Behavior 2nd edn (Oxford Univ. Press, 2010).

  2. Heldstab, S. A., Isler, K., Graber, S. M., Schuppli, C. & van Schaik, C. P. The economics of brain size evolution in vertebrates. Curr. Biol. 32, R697–R708 (2022).

    Article  CAS  PubMed  Google Scholar 

  3. Healy, S. D. in Adaptation and the Brain Ch. 7 (Oxford Univ. Press, 2021).

  4. Dunbar, R. I. M. & Shultz, S. Four errors and a fallacy: pitfalls for the unwary in comparative brain analyses. Biol. Rev. 98, 1278–1309 (2023).

    Article  PubMed  Google Scholar 

  5. Fichtel, C., Henke-von der Malsburg, J. & Kappeler, P. M. Cognitive performance is linked to fitness in a wild primate. Sci. Adv. 9, eadf9365 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  6. Thornton, A. & Lukas, D. Individual variation in cognitive performance: developmental and evolutionary perspectives. Proc. R. Soc. B 367, 2773–2783 (2012).

    Google Scholar 

  7. Croston, R., Branch, C. L., Kozlovsky, D. Y., Dukas, R. & Pravosudov, V. V. Heritability and the evolution of cognitive traits. Behav. Ecol. 26, 1447–1459 (2015).

    Article  Google Scholar 

  8. Plomin, R. et al. Common DNA markers can account for more than half of the genetic influence on cognitive abilities. Psychol. Sci. 24, 562–568 (2013).

    Article  PubMed  Google Scholar 

  9. Rochais, C., Schradin, C. & Pillay, N. Cognitive performance is linked to survival in free-living African striped mice. Proc. R. Soc. B 290, 20230205 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  10. Sonnenberg, B. R., Branch, C. L., Pitera, A. M., Bridge, E. & Pravosudov, V. V. Natural selection and spatial cognition in wild food-caching mountain chickadees. Curr. Biol. 29, 670–676 (2019).

    Article  CAS  PubMed  Google Scholar 

  11. Maille, A. & Schradin, C. Survival is linked with reaction time and spatial memory in African striped mice. Biol. Lett. 12, 20160346 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  12. Dukas, R. & Bernays, E. A. Learning improves growth rate in grasshoppers. Proc. Natl Acad. Sci. USA 97, 2637–2640 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Coomes, J. R. et al. Inhibitory control, exploration behaviour and manipulated ecological context are associated with foraging flexibility in the great tit. J. Anim. Ecol. 91, 320–333 (2022).

    Article  PubMed  Google Scholar 

  14. Nowicki, S. & Searcy, W. A. Song function and the evolution of female preferences: why birds sing, why brains matter. Ann. NY Acad. Sci. 1016, 704–723 (2004).

    Article  PubMed  Google Scholar 

  15. Fine, C. Delusions of Gender (W.W. Norton, 2010).

  16. Buckley, M. G. & Bast, T. A new human delayed-matching-to-place test in a virtual environment reverse-translated from the rodent water maze paradigm: characterization of performance measures and sex differences. Hippocampus 28, 796–812 (2018).

    Article  PubMed  Google Scholar 

  17. Carbia, P. S. & Brown, C. Seasonal variation of sexually dimorphic spatial learning implicates mating system in the intertidal Cocos Frillgoby (Bathygobius cocosensis). Anim. Cogn. 23, 621–628 (2020).

    Article  PubMed  Google Scholar 

  18. Miller, G. The Mating Mind: How Sexual Choice Shaped the Evolution of Human Nature (Doubleday, 2000).

  19. Baur, J., Nsanzimana, J., d’Amour & Berger, D. Sexual selection and the evolution of male and female cognition: a test using experimental evolution in seed beetles. Evolution 73, 2390–2400 (2019).

    Article  PubMed  Google Scholar 

  20. Hollis, B. & Kawecki, T. J. Male cognitive performance declines in the absence of sexual selection. Proc. R. Soc. B 281, 20132873 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  21. Zwoinska, M. K., Lind, M. I., Cortazar‐Chinarro, M., Ramsden, M. & Maklakov, A. A. Selection on learning performance results in the correlated evolution of sexual dimorphism in life history. Evolution 70, 342–357 (2016).

    Article  PubMed  Google Scholar 

  22. Fromhage, L., Jennions, M. D., Myllymaa, L. & Henshaw, J. M. Fitness as the organismal performance measure guiding adaptive evolution. Evolution 78, 1039–1053 (2024).

    Article  PubMed  Google Scholar 

  23. Ashton, B. J., Ridley, A. R., Edwards, E. K. & Thornton, A. Cognitive performance is linked to group size and affects fitness in Australian magpies. Nature 554, 364–367 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Cauchard, L., Boogert, N. J., Lefebvre, L., Dubois, F. & Doligez, B. Problem-solving performance is correlated with reproductive success in a wild bird population. Anim. Behav. 85, 19–26 (2013).

    Article  Google Scholar 

  25. Branch, C. L., Pitera, A. M., Kozlovsky, D. Y., Bridge, E. S. & Pravosudov, V. V. Smart is the new sexy: female mountain chickadees increase reproductive investment when mated to males with better spatial cognition. Ecol. Lett. 22, 897–903 (2019).

    Article  PubMed  Google Scholar 

  26. Preiszner, B. et al. Problem-solving performance and reproductive success of great tits in urban and forest habitats. Anim. Cogn. 20, 53–63 (2017).

    Article  PubMed  Google Scholar 

  27. Johnson-Ulrich, L., Benson-Amram, S. & Holekamp, K. E. Fitness consequences of innovation in spotted hyenas. Front. Ecol. Evol. 7, 443 (2019).

    Article  Google Scholar 

  28. Chen, J., Zou, Y., Sun, Y.-H. & ten Cate, C. Problem-solving males become more attractive to female budgerigars. Science 363, 166–167 (2019).

    Article  CAS  PubMed  Google Scholar 

  29. Chantal, V., Gibelli, J. & Dubois, F. Male foraging efficiency, but not male problem-solving performance, influences female mating preferences in zebra finches. Peer J 4, e2409 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  30. Medina-García, A. & Wright, T. F. An integrative measure of cognitive performance, but not individual task performance, is linked to male reproductive output in budgerigars. Sci. Rep. 11, 11775 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  31. Minter, R., Keagy, J. & Tinghitella, R. M. The relationship between male sexual signals, cognitive performance, and mating success in stickleback fish. Ecol. Evol. 7, 5621–5631 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Isden, J., Panayi, C., Dingle, C. & Madden, J. Performance in cognitive and problem-solving tasks in male spotted bowerbirds does not correlate with mating success. Anim. Behav. 86, 829–838 (2013).

    Article  Google Scholar 

  33. Keagy, J., Savard, J.-F. & Borgia, G. Male satin bowerbird problem-solving ability predicts mating success. Anim. Behav. 78, 809–817 (2009).

    Article  Google Scholar 

  34. Keagy, J., Savard, J.-F. & Borgia, G. Complex relationship between multiple measures of cognitive ability and male mating success in satin bowerbirds, Ptilonorhynchus violaceus. Anim. Behav. 81, 1063–1070 (2011).

    Article  Google Scholar 

  35. Keagy, J., Savard, J.-F. & Borgia, G. Cognitive ability and the evolution of multiple behavioral display traits. Behav. Ecol. 23, 448–456 (2012).

    Article  Google Scholar 

  36. Cole, E. F., Morand-Ferron, J., Hinks, A. E. & Quinn, J. L. Cognitive ability influences reproductive life history variation in the wild. Curr. Biol. 22, 1808–1812 (2012).

    Article  CAS  PubMed  Google Scholar 

  37. Shaw, R. C., MacKinlay, R. D., Clayton, N. S. & Burns, K. C. Memory performance influences male reproductive success in a wild bird. Curr. Biol. 29, 1498–1502 (2019).

    Article  CAS  PubMed  Google Scholar 

  38. White, D. J., Arthur, J., Davies, H. B. & Guigueno, M. F. Cognition and reproductive success in cowbirds. Learn. Behav. 50, 178–188 (2022).

    Article  PubMed  Google Scholar 

  39. Smith, C., Philips, A. & Reichard, M. Cognitive ability is heritable and predicts the success of an alternative mating tactic. Proc. R. Soc. B 282, 20151046 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  40. Bókony, V. et al. Innovative females are more promiscuous in great tits (Parus major). Behav. Ecol. 28, 579–588 (2017).

    Article  Google Scholar 

  41. Head, M. L., Kahn, A. T., Henshaw, J. M., Keogh, J. S. & Jennions, M. D. Sexual selection on male body size, genital length and heterozygosity: consistency across habitats and social settings. J. Anim. Ecol. 86, 1458–1468 (2017).

    Article  PubMed  Google Scholar 

  42. Vega-Trejo, R., Head, M. L., Keogh, J. S. & Jennions, M. D. Experimental evidence for sexual selection against inbred males. J. Anim. Ecol. 86, 394–404 (2017).

    Article  PubMed  Google Scholar 

  43. Harvey, P. D. Domains of cognition and their assessment. Dialogues Clin. Neurosci. 21, 227–237 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  44. Ashton, B. J., Thornton, A., Cauchoix, M. & Ridley, A. R. Long-term repeatability of cognitive performance. R. Soc. Open Sci. 9, 220069 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  45. Soravia, C., Ashton, B. J., Thornton, A. & Ridley, A. R. General cognitive performance declines with female age and is negatively related to fledging success in a wild bird. Proc. R. Soc B 289, 20221748 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  46. Otero, I., Salgado, J. F. & Moscoso, S. Cognitive reflection, cognitive intelligence, and cognitive abilities: a meta-analysis. Intelligence 90, 101614 (2022).

    Article  Google Scholar 

  47. Poirier, M.-A., Kozlovsky, D. Y., Morand-Ferron, J. & Careau, V. How general is cognitive ability in non-human animals? A meta-analytical and multi-level reanalysis approach. Proc. R. Soc. B 287, 20201853 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  48. Braga Goncalves, I., Ashton, B. J. & Fischer, S. Causes and consequences of cognitive variation in fishes. Fishes 8, 277 (2023).

    Article  Google Scholar 

  49. Vinogradov, I. M. et al. The effect of sex, age and boldness on inhibitory control. Anim. Behav. 193, 133–143 (2022).

    Article  Google Scholar 

  50. Wallace, K. J., Rausch, R. T., Ramsey, M. E. & Cummings, M. E. Sex differences in cognitive performance and style across domains in mosquitofish (Gambusia affinis). Anim. Cogn. 23, 655–669 (2020).

    Article  PubMed  Google Scholar 

  51. Vinogradov, I. M., Zang, C., Mahmud-Al-Hasan, M., Head, M. L. & Jennions, M. D. Inbreeding and high developmental temperatures affect cognition and boldness in guppies (Poecilia reticulata). Proc. R. Soc. B 291, 20240785 (2024).

    Article  CAS  PubMed  Google Scholar 

  52. Lucon-Xiccato, T. & Bisazza, A. Sex differences in spatial abilities and cognitive flexibility in the guppy. Anim. Behav. 123, 53–60 (2017).

    Article  Google Scholar 

  53. Prentice, P. M., Mnatzaganian, C., Houslay, T. M., Thornton, A. & Wilson, A. J. Individual differences in spatial learning are correlated across tasks but not with stress response behaviour in guppies. Anim. Behav. 188, 133–146 (2022).

    Article  Google Scholar 

  54. Agrillo, C., Miletto Petrazzini, M. E., Piffer, L., Dadda, M. & Bisazza, A. A new training procedure for studying discrimination learning in fish. Behav. Brain Res. 230, 343–348 (2012).

    Article  PubMed  Google Scholar 

  55. Trompf, L. & Brown, C. Personality affects learning and trade-offs between private and social information in guppies, Poecilia reticulata. Anim. Behav. 88, 99–106 (2014).

    Article  Google Scholar 

  56. Polverino, G., Ruberto, T., Staaks, G. & Mehner, T. Tank size alters mean behaviours and individual rank orders in personality traits of fish depending on their life stage. Anim. Behav. 115, 127–135 (2016).

    Article  Google Scholar 

  57. Vinogradov, I. Cognitive Abilities in Fish: Biological Predictors and Impact on Reproductive Success. PhD thesis, Australian National University (2024)

  58. Dougherty, L. R. & Guillette, L. M. Linking personality and cognition: a meta-analysis. Proc. R. Soc. B 373, 20170282 (2018).

    Google Scholar 

  59. Aich, U., Bonnet, T., Head, M. L. & Jennions, M. D. Disentangling the effects of male age and mating history: contrasting effects of mating history on precopulatory mating behavior and paternity success. Evolution 75, 2867–2880 (2021).

    Article  PubMed  Google Scholar 

  60. Iglesias-Carrasco, M., Fox, R. J., Vega-Trejo, R., Jennions, M. D. & Head, M. L. An experimental test for body size-dependent effects of male harassment and an elevated copulation rate on female lifetime fecundity and offspring performance. J. Evol. Biol. 32, 1262–1273 (2019).

    Article  PubMed  Google Scholar 

  61. Head, M. L., Vega-Trejo, R., Jacomb, F. & Jennions, M. D. Predictors of male insemination success in the mosquitofish (Gambusia holbrooki). Ecol. Evol. 5, 4999–5006 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  62. Kim, B., Moran, N. P., Reinhold, K. & Sánchez-Tójar, A. Male size and reproductive performance in three species of livebearing fishes (Gambusia spp.): a systematic review and meta-analysis. J. Anim. Ecol. 90, 2431–2445 (2021).

    Article  PubMed  Google Scholar 

  63. Vieira, V. Permutation tests to estimate significances on principal components analysis. Comput. Ecol. Softw. 2, 103–123 (2012).

    Google Scholar 

  64. Janicke, T., Häderer, I. K., Lajeunesse, M. J. & Anthes, N. Darwinian sex roles confirmed across the animal kingdom. Sci. Adv. 2, e1500983 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  65. Rice, W. R. & Gaines, S. D. Heads I win, tails you lose: testing directional alternative hypotheses in ecological and evolutionary research. Trends Ecol. Evol. 9, 235–237 (1994).

    Article  CAS  PubMed  Google Scholar 

  66. Agrillo, C., Dadda, M. & Bisazza, A. Sexual harassment influences group choice in female mosquitofish. Ethology 112, 592–598 (2006).

    Article  Google Scholar 

  67. 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 (2017).

    Article  Google Scholar 

  68. Birkhead, T. R. & Pizzari, T. Postcopulatory sexual selection. Nat. Rev. Genet. 3, 262–273 (2002).

    Article  CAS  PubMed  Google Scholar 

  69. Reznick, D., Nunney, L. & Tessier, A. Big houses, big cars, superfleas and the costs of reproduction. Trends Ecol. Evol. 15, 421–425 (2000).

    Article  CAS  PubMed  Google Scholar 

  70. Haig, D. The strategic gene. Biol. Philos. 27, 461–479 (2012).

    Article  Google Scholar 

  71. Sober, E. The Nature of Selection (Chicago Univ. Press, 1984).

  72. Herdegen-Radwan, M. Can female guppies learn to like male colours? A test of the role of associative learning in originating sexual preferences. Proc. R. Soc. B 289, 20220212 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Lucon-Xiccato, T., Manabe, K. & Bisazza, A. Guppies learn faster to discriminate between red and yellow than between two shapes. Ethology 125, 82–91 (2019).

    Article  Google Scholar 

  74. Lucon-Xiccato, T. & Bisazza, A. Discrimination reversal learning reveals greater female behavioural flexibility in guppies. Biol. Lett. 10, 20140206 (2014).

    Article  PubMed Central  Google Scholar 

  75. Ariyomo, T. O. & Watt, P. J. The effect of variation in boldness and aggressiveness on the reproductive success of zebrafish. Anim. Behav. 83, 41–46 (2012).

    Article  Google Scholar 

  76. Vargas, R., Mackenzie, S. & Rey, S. Love at first sight: the effect of personality and colouration patterns in the reproductive success of zebrafish (Danio rerio). PLoS ONE 13, e0203320 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  77. Scherer, U., Godin, J.-G. J. & Schuett, W. Do female rainbow kribs choose males on the basis of their apparent aggression and boldness? A non-correlational mate choice study. Behav. Ecol. Sociobiol. 74, 34 (2020).

    Article  Google Scholar 

  78. Chapman, J. R., Nakagawa, S., Coltman, D. W., Slate, J. & Sheldon, B. C. A quantitative review of heterozygosity–fitness correlations in animal populations. Mol. Ecol. 18, 2746–2765 (2009).

    Article  CAS  PubMed  Google Scholar 

  79. Marsh, J. N., Vega‐Trejo, R., Jennions, M. D. & Head, M. L. Why does inbreeding reduce male paternity? Effects on sexually selected traits. Evolution 71, 2728–2737 (2017).

    Article  PubMed  Google Scholar 

  80. Nepoux, V., Haag, C. R. & Kawecki, T. J. Effects of inbreeding on aversive learning in Drosophila. J. Evol. Biol. 23, 2333–2345 (2010).

    Article  CAS  PubMed  Google Scholar 

  81. Richardson, J., Comin, P. & Smiseth, P. T. Inbred burying beetles suffer fitness costs from making poor decisions. Proc. R. Soc. B 285, 20180419 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  82. Abu-Rabia, S. & Maroun, L. The effect of consanguineous marriage on reading disability in the Arab community. Dyslexia 11, 1–21 (2005).

    Article  PubMed  Google Scholar 

  83. Bashi, J. Effects of inbreeding on cognitive performance. Nature 266, 440–442 (1977).

    Article  CAS  PubMed  Google Scholar 

  84. Fareed, M. & Afzal, M. Estimating the inbreeding depression on cognitive behavior: a population-based study of child cohort. PLoS ONE 9, e109585 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  85. C Yuen, R. K. et al. Whole genome sequencing resource identifies 18 new candidate genes for autism spectrum disorder. Nat. Neurosci. 20, 602–611 (2017).

    Article  PubMed  Google Scholar 

  86. Hughes, R. B., Whittingham-Dowd, J., Clapcote, S. J., Broughton, S. J. & Dawson, N. Altered medial prefrontal cortex and dorsal raphé activity predict genotype and correlate with abnormal learning behavior in a mouse model of autism-associated 2p16.3 deletion. Autism Res. 15, 614–627 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  87. Troy Harker, K. & Whishaw, I. Q. Place and matching-to-place spatial learning affected by rat inbreeding (Dark–Agouti, Fischer 344) and albinism (Wistar, Sprague–Dawley) but not domestication (wild rat vs. Long–Evans, Fischer–Norway). Behav. Brain Res. 134, 467–477 (2002).

    Article  PubMed  Google Scholar 

  88. Sheldon, B. C., Kruuk, L. E. B. & Alberts, S. C. The expanding value of long-term studies of individuals in the wild. Nat. Ecol. Evol. 6, 1799–1801 (2022).

    Article  PubMed  Google Scholar 

  89. Frankham, R., Briscoe, D. A. & Ballou, J. D. Introduction to Conservation Genetics (Cambridge Univ. Press, 2002).

  90. Keller, L. F. Inbreeding and its fitness effects in an insular population of song sparrows (Melospiza melodia). Evolution 52, 240–250 (1998).

    PubMed  Google Scholar 

  91. Aellen, M., Burkart, J. M. & Bshary, R. No evidence for general intelligence in a fish. Ethology 128, 424–436 (2022).

    Article  Google Scholar 

  92. Burkart, J. M., Schubiger, M. N. & van Schaik, C. P. The evolution of general intelligence. Behav. Brain Sci. 40, e195 (2017).

    Article  PubMed  Google Scholar 

  93. Maille, A. & Schradin, C. Ecophysiology of cognition: how do environmentally induced changes in physiology affect cognitive performance? Biol. Rev. 92, 1101–1112 (2017).

    Article  PubMed  Google Scholar 

  94. Cummings, M. E. Sexual conflict and sexually dimorphic cognition—reviewing their relationship in poeciliid fishes. Behav. Ecol. Sociobiol. 72, 73 (2018).

    Article  Google Scholar 

  95. Cabral, J. A. & Marques, J. C. Life history, population dynamics and production of eastern mosquitofish, Gambusia holbrooki (Pisces, Poeciliidae), in rice fields of the lower Mondego River Valley, western Portugal. Acta Oecologica 20, 607–620 (1999).

    Article  Google Scholar 

  96. Caldwell, M. C. & Caldwell, D. K. Monarchistic dominance in small groups of captive male mosquitofish, Gambusia affinis patruelis. Bull. South. Calif. Acad. Sci. 61, 37–43 (1962).

    Google Scholar 

  97. Harrison, L. M., Jennions, M. D. & Head, M. L. Does the winner–loser effect determine male mating success? Biol. Lett. 14, 20180195 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  98. Bisazza, A. & Marin, G. Sexual selection and sexual size dimorphism in the eastern mosquitofish Gambusia holbrooki (Pisces Poeciliidae). Ethol. Ecol. Evol. 7, 169–183 (1995).

    Article  Google Scholar 

  99. Zane, N. & Jones, A. Microsatellite assessment of multiple paternity in natural populations of a live‐bearing fish, Gambusia holbrooki. J. Evol. Biol. 12, 61–69 (1999).

    Article  Google Scholar 

  100. Bisazza, A., Pignatti, R. & Vallortigara, G. Detour tests reveal task- and stimulus-specific behavioural lateralization in mosquitofish (Gambusia holbrooki). Behav. Brain Res. 89, 237–242 (1997).

    Article  CAS  PubMed  Google Scholar 

  101. Vinogradov, I. M., Jennions, M. D., Neeman, T. & Fox, R. J. Repeatability of lateralisation in mosquitofish Gambusia holbrooki despite evidence for turn alternation in detour tests. Anim. Cogn. 24, 765–775 (2021).

    Article  PubMed  Google Scholar 

  102. Wilson, R. S. Temperature influences the coercive mating and swimming performance of male eastern mosquitofish. Anim. Behav. 70, 1387–1394 (2005).

    Article  Google Scholar 

  103. Davidson, G. L. et al. Inhibitory control performance is repeatable over time and across contexts in a wild bird population. Anim. Behav. 187, 305–318 (2022).

    Article  Google Scholar 

  104. Boogert, N. J., Anderson, R. C., Peters, S., Searcy, W. A. & Nowicki, S. Song repertoire size in male song sparrows correlates with detour reaching, but not with other cognitive measures. Anim. Behav. 81, 1209–1216 (2011).

    Article  Google Scholar 

  105. Lucon-Xiccato, T., Montalbano, G., Reddon, A. R. & Bertolucci, C. Social environment affects inhibitory control via developmental plasticity in a fish. Anim. Behav. 183, 69–76 (2022).

    Article  Google Scholar 

  106. Prentice, P. M., Thornton, A., Kolm, N. & Wilson, A. J. Genetic and context-specific effects on individual inhibitory control performance in the guppy (Poecilia reticulata). J. Evol. Biol. 36, 1796–1810 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Brandão, M. L., Fernandes, A. M. T., de, A. & Gonçalves-de-Freitas, E. Male and female cichlid fish show cognitive inhibitory control ability. Sci. Rep. 9, 15795 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  108. van Horik, J. O. et al. Do detour tasks provide accurate assays of inhibitory control? Proc. R. Soc. B 285, 20180150 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  109. Lucon-Xiccato, T., Gatto, E. & Bisazza, A. Fish perform like mammals and birds in inhibitory motor control tasks. Sci. Rep. 7, 13144 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  110. Brown, C. & Braithwaite, V. A. Effects of predation pressure on the cognitive ability of the poeciliid Brachyraphis episcopi. Behav. Ecol. 16, 482–487 (2005).

    Article  Google Scholar 

  111. Kilian, A. et al. in Data Production and Analysis in Population Genomics: Methods and Protocols (eds Pompanon, F. & Bonin, A.) 67–89 (Humana Press, 2012).

  112. Booksmythe, I., Head, M. L., Keogh, J. S. & Jennions, M. D. Fitness consequences of artificial selection on relative male genital size. Nat. Commun. 7, 11597 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Spagopoulou, F., Vega-Trejo, R., Head, M. L. & Jennions, M. D. Shifts in reproductive investment in response to competitors lower male reproductive success. Am. Nat. 196, 355–365 (2020).

    Article  PubMed  Google Scholar 

  114. Paternity analysis reveals sexual selection on cognitive performance. Figshare https://figshare.com/s/4cc0aeaa01188668c0e7 (2025).

  115. R Core Team R: The R Project for Statistical Computing (R Foundation for Statistical Computing, 2022); https://www.r-project.org/

  116. Brooks, M. E. et al. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modelling. R J 9, 378–400 (2017).

    Article  Google Scholar 

  117. Bates, D. et al. lme4: Linear mixed-effects models using ‘Eigen’ and S4. R package version 1.1.30 (2023).

  118. Hartig, F. DHARMa: Residual diagnostics for hierarchical (multi-level/mixed) regression models. R package version 0.4.6 (2022).

  119. Lüdecke, D., Ben-Shachar, M. S., Patil, I., Waggoner, P. & Makowski, D. performance: an R package for assessment, comparison and testing of statistical models. J. Open Source Softw. 6, 3139 (2021).

    Article  Google Scholar 

  120. Camargo, A. PCAtest: testing the statistical significance of principal component analysis in R. Peer J. 10, e12967 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  121. Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank the ANU Animal Services staff, U. Aich, M.-H. Chung and L. Harrison for assistance with fish husbandry. We thank T. Neeman for assistance with statistical analysis. We thank the Australian Research Council (DP2019100279) and the German Primate Centre for funding. We extend special thanks to A. Kilian from DaRT for providing genotyping services at a generously discounted rate.

Author information

Authors and Affiliations

  1. Division of Ecology & Evolution, Research School of Biology, The Australian National University, Canberra, Australian Capital Territory, Australia

    Ivan M. Vinogradov, Rebecca J. Fox & Michael D. Jennions

  2. Behavioral Ecology and Sociobiology Unit, German Primate Center, Leibniz Institute for Primate Research, Göttingen, Germany

    Claudia Fichtel & Peter M. Kappeler

  3. Department of Sociobiology/Anthropology, Johann-Friedrich-Blumenbach Institute of Zoology and Anthropology, University of Göttingen, Göttingen, Germany

    Peter M. Kappeler

  4. Stellenbosch Institute for Advanced Study (STIAS), Wallenberg Research Centre at Stellenbosch University, Stellenbosch, South Africa

    Michael D. Jennions

Authors
  1. Ivan M. Vinogradov
    View author publications

    Search author on:PubMed Google Scholar

  2. Rebecca J. Fox
    View author publications

    Search author on:PubMed Google Scholar

  3. Claudia Fichtel
    View author publications

    Search author on:PubMed Google Scholar

  4. Peter M. Kappeler
    View author publications

    Search author on:PubMed Google Scholar

  5. Michael D. Jennions
    View author publications

    Search author on:PubMed Google Scholar

Contributions

All authors conceived and designed the study. I.M.V. and R.J.F. collected and analysed the data. All authors interpreted the data, co-wrote the paper and gave permission for publication.

Corresponding author

Correspondence to Ivan M. Vinogradov.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Ecology & Evolution thanks the anonymous reviewers for their contribution to the peer review of this work. Peer reviewer reports are available.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Null PCA distributions calculated from 10 000 simulated data sets using PCAtest package in R120 and empirical statistics from measurements of cognitive abilities in mosquitofish (n = 63).

Grey and red points represent random permutations and mean observed values, respectively, with error-bars showing 95% confidence intervals (CI).

Extended Data Fig. 2 Linear relationship between principal component 1 (PC1) and the composite cognitive score (CCS) for cognitive measures in male mosquitofish Gambusia holbrooki.

CCS was calculated as the mean of the standardised values for spatial learning, associative learning, reversal learning, and a standardised combined mean of inhibitory control and initial impulse time.

Extended Data Fig. 3 Histogram of the number of offspring sired per male (A) and produced per female (B) by mosquitofish Gambusia holbrooki in 11 mating ponds.

Each pond initially had 7-11 males and an equal number of virgin females.

Supplementary information

Supplementary Information

Supplementary Tables 1–7 and Figs. 1–3.

Reporting Summary

Peer review File

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vinogradov, I.M., Fox, R.J., Fichtel, C. et al. Paternity analysis reveals sexual selection on cognitive performance in mosquitofish. Nat Ecol Evol 9, 692–704 (2025). https://doi.org/10.1038/s41559-025-02645-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue date:

  • DOI: https://doi.org/10.1038/s41559-025-02645-3

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing