Sexual conflict and sexually dimorphic cognition—reviewing their relationship in poeciliid fishes

  • Molly E. Cummings
Part of the following topical collections:
  1. From sensory perception to behavior


Sexual conflict, the difference in preferred mating rates between the sexes, often leads to sexually dimorphic morphologies, strategies, and behaviors. We are now beginning to realize that this pervasive evolutionary process has implications for variation in cognition as well. Here, I review the evidence for this in poeciliid fishes with a focus on taxa that exhibit high levels of sexual conflict (Gambusia affinis, G. holbrooki, Poecilia reticulata) as well as taxa that represent a more moderate level of sexual conflict (Xiphophorus nigrensis). Sexually dimorphic behaviors emerge across poeciliids in predictable directions consistent with sexual conflict and associated with sex-specific variation in cognition. For instance, poeciliid females have evolved a suite of behaviors that reduce male harassment, including greater shoaling tendencies and risk sensitivities than males. Meanwhile, cognitive styles and cognitive-behavioral profiles diverge between the sexes in ways that highlight these behavioral differences likely born from conflict. Male and female G. affinis have opposing relationships between exploratory tendencies and learning, and they also exhibit distinct behavioral predictors (sociability, activity, anxiety, and exploratory behaviors) for individual learning performance. Artificial selection studies suggest that increases in sexual conflict lead to a demand in cognitive processes; and neurogenomic studies reveal that specific brain regions and molecular pathways underlying high and low sexual conflict interactions may differ. While the current body of evidence is still nascent in many respects, I will highlight areas of research in which further investigation with poeciliid fishes can provide insight into the intertwined relationship between sexual conflict and cognition.

Significance statement

Rarely does one consider the benefits of conflict. However, when it comes to sexual conflict, one of the potential benefits it may bring is advances in cognition. I use the poeciliid fishes to showcase this idea as they are both a model for sexual conflict and an experimentally tractable system to test for cognitive variation. I review the current evidence across poeciliid fishes that sexual conflict drives behavioral changes, physiological investment in brain size, and neuromolecular responses within the brain. Furthermore, I examine sexually dimorphic relationships between learning performance and behavioral traits. While all the data reported in this review come from poeciliid fishes, the evolutionarily conserved nature of the decision-making network across vertebrate brains suggests the reported patterns may have relevance to a diversity of vertebrates (including humans) that experience high degrees of sexual conflict.


Sexual selection Courtship Coercion Reproductive strategies Coevolution Brain 



The author would like to thank three highly constructive and patient reviewers along with all current and previous undergraduates, graduate students, and postdocs who have contributed in poeciliid behavioral, cognitive, and neurogenomic research in my lab over the past decade.

Funding information

This research was conducted with previous external financial support from NSF (IOS-0813742 and IOS-0843000). This research also received financial support from BEACON.

Compliance with ethical standards

Conflict of interest

The author declares she has no conflict of interest.

Ethical approval

All applicable international, national, and institutional guidelines for the care and use of animals were followed as outlined in our IACUC protocol (AUP-2016-00246).

Data availability

Data sharing not applicable to this article as no datasets were generated or analyzed during the current study.


  1. Abrahams MV (1989) Foraging guppies and the ideal free distribution: the influence of information on patch choice. Ethology 82:116–126CrossRefGoogle Scholar
  2. Agrillo C, Miletto Petrazzini ME, Bisazza A (2017) Numerical abilities in fish: a methodological review. Behav Process 141:161–171CrossRefGoogle Scholar
  3. Arnqvist G, Rowe L (2002) Antagonistic coevolution between the sexes in a group of insects. Nature 415:787–789CrossRefPubMedGoogle Scholar
  4. Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, PrincetonCrossRefGoogle Scholar
  5. Bateman A (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368CrossRefPubMedGoogle Scholar
  6. Bisazza A (1993) Male competition, female mate choice and sexual size dimorphism in poeciliid fishes. In: Huntingford FA, Torricelli P (eds) The Behavioural ecology of fishes. Harwood Academic publishers, Chur, pp 257–286Google Scholar
  7. Bisazza A, Pilastro A (1997) Small male mating advantage and reversed size dimorphism in poeciliid fishes. J Fish Biol 50:397–406CrossRefGoogle Scholar
  8. Bisazza A, Pignatti R, Vallortigara G (1997) Laterality in detour behaviour: interspecific variation in poeciliid fish. Anim Behav 54(5):1273–1281CrossRefPubMedGoogle Scholar
  9. Bisazza A, Facchin L, Pignatti R, Vallortigara G (1998) Lateralization of detour behaviour in poeciliid fish: The effect of species, gender and sexual motivation. Behav Brain Res 91(1-2):157–164CrossRefPubMedGoogle Scholar
  10. Booksmythe I, Head ML, Keogh S, Jennions MD (2016) Fitness consequences of artificial selection on relative male genital size. Nat Commun 7:11597CrossRefPubMedPubMedCentralGoogle Scholar
  11. Brennan PLR, Prum RO (2014) Mechanisms and evidence of genital coevolution: the roles of natural selection, mate choice and sexual conflict. In: Rice WR, Gavrilets S (eds) The genetics and biology of sexual conflict. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 385–405Google Scholar
  12. Bshary R, Gingins S, Vail AL (2014) Social cognition in fishes. Trends Cogn Sci 18:465–471CrossRefPubMedGoogle Scholar
  13. Buechel SD, Booksmythe I, Kotrschal A, Jennions MD, Kolm N (2016) Artificial selection on male genitalia length alters female brain size. Proc R Soc B 282:20161796CrossRefGoogle Scholar
  14. Burns JG, Rodd FH (2008) Hastiness, brain size and predation regime affect the performance of wild guppies in a spatial memory task. Anim Behav 76:911–922CrossRefGoogle Scholar
  15. Clark E, Aronson LR, Gordon M (1954) Mating behavior patterns in two sympatric species of xiphophorin fishes: their inheritance and significance in sexual isolation. Bull Am Mus Nat Hist 103:135–226Google Scholar
  16. Constanz GD (1989) Reproductive biology of poeciliid fishes. In: Meffe GK, Snelson FF (eds) Ecology and evolution of livebearing fishes (Poecliidae). Prentice Hall, Englewood Cliffs, pp 33–50Google Scholar
  17. Correl-Lopez A, Bloch NI, Kotrschal A, van der Bijl W, Bueschel SD, Mank JE, Kolm N (2017) Female brain size affects the assessment of male attractiveness during mate choice. Sci Adv 3:e1601990CrossRefGoogle Scholar
  18. Cote J, Fogarty S, Weinersmith K, Brodin T, Sih A (2010) Personality traits and dispersal tendency in the invasive mosquitofish (Gambusia affinis). Proc R Soc B Biol Sci 277(1687):1571–1579CrossRefGoogle Scholar
  19. Croft DP, Albanese B, Arrowsmith BJ, Botham M, Webster M, Krause J (2003) Sex biased movement in the guppy (Poecilia reticulata). Oecologia 137:62–68CrossRefPubMedGoogle Scholar
  20. Croft DP, Morrell LJ, Wade AS, Piyapong C, Ioannou CC, Dyer JRG, Champman BB, Yan W, Krause J (2006) Predation risk as a driving force for sexual segregation: a cross-population comparison. Am Nat 167:867–878PubMedGoogle Scholar
  21. Culumber ZW, Tobler M (2017) Sex-specific evolution during the diversification of live-bearing fishes. Nat Ecol Evol 1:1185–1191CrossRefPubMedGoogle Scholar
  22. Cummings ME (2012) Looking for sexual selection in the female brain. Philos T Roy Soc B 367:2348–2356CrossRefGoogle Scholar
  23. Cummings ME (2015) The mate choice mind: studying mate preference, aversion and social cognition in the female poeciliid brain. Anim Behav 103:249–258CrossRefGoogle Scholar
  24. Cummings ME, Mollaghan DM (2006) Repeatability and consistency of female preference behaviours in a northern swordtail, Xiphophorus nigrensis. Anim Behav 72:217–224CrossRefGoogle Scholar
  25. Cummings ME, Ramsey ME (2015) Mate choice as social cognition: predicting behavioral and neural plasticity as a function of mating system. Curr Opin Behav Sci 6:125–131CrossRefGoogle Scholar
  26. Cummings ME, Larkins-Ford J, Reilly CRL, Wong RY, Ramsey ME, Hofmann HA (2008) Sexual and social stimuli elicit rapid and contrasting genomic responses. Proc R Soc Lond B 275:393–402CrossRefGoogle Scholar
  27. Dadda M (2015) Female social response to male sexual harassment in poeciliid fish: a comparison of six species. Front Psychol 6:1453CrossRefPubMedPubMedCentralGoogle Scholar
  28. Dadda M, Pilastro A, Bisazza A (2005) Male sexual harassment and female schooling behaviour in the eastern mosquitofish. Anim Behav 70:463–471CrossRefGoogle Scholar
  29. Darden SK, Croft DP (2008) Male harassment drives females to alter habitat use and leads to segregation of the sexes. Biol Lett 4:449–451CrossRefPubMedPubMedCentralGoogle Scholar
  30. DePasquale C, Wagner T, Archard GA, Ferguson B, Braithwaite VA (2014) Learning rate and temperament in a high predation risk environment. Oecologia 176:661–667CrossRefPubMedPubMedCentralGoogle Scholar
  31. Dugatkin LA, Alfieri MS (2003) Boldness, behavioral inhibition and learning. Ethol Ecol Evol 15:43–49CrossRefGoogle Scholar
  32. Dunbar RIM, Schultz S (2007) Evolution of the social brain. Science 317:1344–1347CrossRefPubMedGoogle Scholar
  33. Dussault GV, Kramer DL (1981) Food and feeding behaviour of the guppy, Poecilia reticulata (Pisces: Poeciliidae). Can J Zool 59:684–701CrossRefGoogle Scholar
  34. Endler JA (1987) Predation, light intensity and courtship behaviour in Poecilia reticulata (Pisces: Poeciliidae). Anim Behav 35:1376–1385CrossRefGoogle Scholar
  35. Etheredge RI, Avenas C, Armstrong MJ, Cummings ME (2018) Sex-specific cognitive-behavioural profiles emerging from individual variation in numerosity discrimination in Gambusia affinis. Anim Cogn 21:37–53CrossRefPubMedGoogle Scholar
  36. Evans JP, Magurran AE (2001) Patterns of sperm precedence and predictors of paternity in the Trinidadian guppy. Proc R Soc Lond B 268:719–724CrossRefGoogle Scholar
  37. Farr JA (1989) Sexual selection and secondary sexual differentiation in poeciliids: determinants of male mating success and the evolution of female choice. Prentice Hall, Englewood CliffsGoogle Scholar
  38. Gaulin SJC, Fitzgerald RW (1989) Sexual selection for spatial-learning ability. Anim Behav 37:322–331CrossRefGoogle Scholar
  39. Greven H (2005) Structural and behavioral traits associated with sperm transfer in Poeciliinae. In: Grier HJ, Uribe MC (eds) Viviparous fishes. New Life Publication, Homestead, pp 145–163Google Scholar
  40. Guillette LM, Reddon AR, Hurd PL, Sturdy CB (2009) Exploration of a novel space is associated with individual differences in learning speed in a novel space is associated with individual differences in learning speed in black-capped chickadees, Poecile atricapillus. Behav Process 82:265–270CrossRefGoogle Scholar
  41. Head ML, Kahn AT, Henshaw JM, Keogh JS, Jennions MD (2017) Sexual selection on male body size, genital length and heterozygosity: consistency across habitats and social settings. J Anim Ecol 86:1458–1468CrossRefPubMedGoogle Scholar
  42. Heinen-Kay JL, Schmidt DA, Stafford AT, Costa MT, Pererson MN, Kern EMA, Langerhans B (2016) Predicting multifarious behavioural divergence in the wild. Anim Behav 121:3–10CrossRefGoogle Scholar
  43. Holland B, Rice WR (1999) Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes a reproductive load. Proc Natl Acad Sci USA 96:5083–5088CrossRefPubMedGoogle Scholar
  44. Houde AE (1997) Sex, color and mate choice in guppies. Princeton University Press, PrincetonGoogle Scholar
  45. Jones CM, Braithwaite VA, Healy SD (2003) The evolution of sex differences in spatial ability. Behav Neurosci 117:403–411CrossRefPubMedGoogle Scholar
  46. Jones JC, Fruciano C, Keller A, Schartl M, Meyer A (2016) Evolution of the elaborate male intromittent organ of Xiphophorus fishes. Ecol Evol 6:7207–7220CrossRefPubMedPubMedCentralGoogle Scholar
  47. Kotrschal A, Räsänen K, Kristjánsson BK, Senn M, Kolm N (2012) Extreme sexual brain size dimorphism in sticklebacks: a consequence of the cognitive challenges of sex and parenting? PLoS One 7:e30055CrossRefPubMedPubMedCentralGoogle Scholar
  48. Kotrschal A, Rogell B, Bundsen A, Svensson B, Zajitschek S, Brannstrom I, Immler S, Maklakov AA, Kom N (2013) Artificial selection on relative brain size in the guppy reveals costs and benefits of evolving a larger brain. Curr Biol 23:168–171CrossRefPubMedPubMedCentralGoogle Scholar
  49. Kotrschal A, Buechel SD, Zala SM, Corral-Lopez A, Penn DJ, Kolm N (2015a) Brain size affects female but not male survival under predation threat. Ecol Lett 18:646–652CrossRefPubMedPubMedCentralGoogle Scholar
  50. Kotrschal A, Corral-Lopez A, Zajitschek S, Immler S, Maklakov AA, Kolm N (2015b) Positive genetic correlation between brain size and sexual traits in male guppies artificially selected for brain size. J Evol Biol 28:841–850CrossRefPubMedPubMedCentralGoogle Scholar
  51. Kotrschal A, Corral-Lopez A, Amcoff M, Kolm N (2015c) A larger brain confers a benefit in a spatial mate search learning task in male guppies. Behav Ecol 26:527–532CrossRefPubMedGoogle Scholar
  52. Kwan L, Cheng YY, Rodd FH, Rowe L (2013) Sexual conflict and the function of genitalic claws in guppies (Poecilia reticulata). Biol Lett 9:20130267CrossRefPubMedPubMedCentralGoogle Scholar
  53. Laland KN, Reader SM (1999a) Foraging innovation in the guppy. Anim Behav 57:331–340CrossRefPubMedGoogle Scholar
  54. Laland KN, Reader SM (1999b) Foraging innovation is inversely related to competitive ability in male but not in female guppies. Behav Ecol 10:270–274CrossRefGoogle Scholar
  55. Langerhans BR (2010) Predicting evolution with generalized models of divergent selection: a case study with poeciliid fish. Integr Comp Biol 50:1167–1184CrossRefPubMedGoogle Scholar
  56. Langerhans BR (2011) Genital evolution. In: Evans JP, Pilastro A, Schlupp I (eds) Ecology and evolution of poeciliid fishes. University of Chicago Press, Chicago, pp 228–240Google Scholar
  57. Lucon-Xiccato T, Bisazza A (2014) Discrimination reversal learning reveals greater female behavioural flexibility in guppies. Biol Lett 10:20140206CrossRefPubMedCentralGoogle Scholar
  58. Lucon-Xiccato T, Bisazza A (2016) Male and female guppies differ in speed but not in accuracy in visual discrimination learning. Anim Cogn 19:733–744CrossRefPubMedGoogle Scholar
  59. Lucon-Xiccato T, Bisazza A (2017a) Individual differences in cognition among teleost fishes. Behav Process 141:184–195CrossRefGoogle Scholar
  60. Lucon-Xiccato T, Bisazza A (2017b) Sex differences in spatial abilities and cognitive flexibility in the guppy. Anim Behav 123:53–60CrossRefGoogle Scholar
  61. Lucon-Xiccato T, Dadda M (2016) Guppies show behavioural but not cognitive sex differences in a novel object recognition test. PLoS One 11:e0156589CrossRefPubMedPubMedCentralGoogle Scholar
  62. Lynch KS, Ramsey ME, Cummings ME (2012) The mate choice brain: comparing gene profiles between female choice and male coercive poeciliids. Genes Brain Behav 11:222–229CrossRefPubMedGoogle Scholar
  63. MacLean EL, Hare B, Nunn CL et al (2014) The evolution of self-control. P Natl Acad Sci USA 111:E2140–E2148CrossRefGoogle Scholar
  64. Magurran AE (2011) Sexual coercion. In: Evans JP, Pilastro A, Schlupp I (eds) Ecology and evolution of poeciliid fishes. Chicago University Press, Chicago, pp 209–216Google Scholar
  65. Magurran AE, Maciás Garcia C (2000) Sex differences in behaviour as an indirect consequence of mating system. J Fish Biol 57:839–857CrossRefGoogle Scholar
  66. Magurran AE, Nowak MA (1991) Another battle of the sexes: the consequences of sexual asymmetry in mating costs and predation risk in the guppy, Poecilia reticulata. Proc R Soc Lond B 246:31–38CrossRefGoogle Scholar
  67. Magurran AE, Seghers BH (1994a) Sexual conflict as a consequence of ecology: evidence from guppy, Poecilia reticulata, populations in Trinidad. Proc R Soc Lond B 255:31–36CrossRefGoogle Scholar
  68. Magurran AE, Seghers BH (1994b) A cost of sexual harassment in the guppy, Poecilia reticulata. Proc R Soc Lond B 258:89–92CrossRefGoogle Scholar
  69. Matta R, Ervin KSJ, Choleris E (2016) The neurobiology of social learning. In: Olmstead MC (ed) Animal cognition: principles, evolution, and development, 1st edn. Nova Science Publishers, Hauppauge, pp 171–200Google Scholar
  70. Mautz BS, Jennions MD (2011) The effect of competitor presence and relative competitive ability on male mate choice. Behav Ecol 22:261–267CrossRefGoogle Scholar
  71. Maximino C, Marques de Brito T, Dias CA, Jr GA, Morato S (2010) Scototaxis as anxiety-like behavior in fish. Nat Protoc 5:209–216CrossRefPubMedGoogle Scholar
  72. O’Connell LA, Hofmann HA (2011) The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J Comp Neurol 519:3599–3639CrossRefPubMedGoogle Scholar
  73. O’Connell LA, Hofmann HA (2012) Evolution of a vertebrate social-decision making network. Science 336:1154–1157CrossRefPubMedGoogle Scholar
  74. Parker GA (1979) Sexual selection and reproductive competition in insects. Academic Press, New YorkGoogle Scholar
  75. Parker GA (2006) Sexual conflict over mating and fertilization: an overview. Philos T Roy Soc B 361:235–259CrossRefGoogle Scholar
  76. Parzefall J (1973) Attraction and sexual cycle of poeciliids. In: Schröder JH (ed) Genetics and mutagenesis of fish. Springer-Verlag, Berlin, pp 357–406Google Scholar
  77. Pilastro A, Bisazza A (1999) Insemination efficiency of two alternative male mating tactics in the guppy (Poecilia reticulata). Proc R Soc Lond B 266:1887–1891CrossRefGoogle Scholar
  78. Pilastro A, Giacomello E, Bisazza A (1997) Sexual selection for small size in male mosquitofish (Gambusia holbrooki). Proc R Soc Lond B 264:1125–1129CrossRefGoogle Scholar
  79. Pilastro A, Benetton S, Bisazza A (2003) Female aggregation and male competition reduce costs of sexual harassment in the mosquitofish Gambusia holbrooki. Anim Behav 65:1161–1167CrossRefGoogle Scholar
  80. Pollux BJA, Meredith RW, Springer MS, Garland T, Reznick DN (2014) The evolution of the placenta drives a shift in sexual selection in livebearing fish. Nature 513:233–236CrossRefPubMedGoogle Scholar
  81. Ptacek MB, Travis J (1998) Hierarchical patterns of covariance between morphological and behavioural traits. Anim Behav 56:1044–1048CrossRefPubMedGoogle Scholar
  82. Ramsey ME, Maginnis TL, Wong RY, Brock C, Cummings ME (2012) Identifying context-specific gene profiles of social, reproductive and mate preference behavior in a fish species with female mate choice. Front Neurosci 6:62CrossRefPubMedPubMedCentralGoogle Scholar
  83. Ramsey ME, Vu W, Cummings ME (2014) Testing synaptic plasticity in dynamic mate choice decisions: N-methyl D-aspartate receptor blockade disrupts female preference. Proc R Soc B 281:20140047CrossRefPubMedGoogle Scholar
  84. Reznick D (1983) The structure of guppy life histories: the tradeoff between growth and reproduction. Ecology 64:862–873CrossRefGoogle Scholar
  85. Rice WR (1996) Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381:232–234CrossRefPubMedGoogle Scholar
  86. Rosenthal GG (2017) Mate choice: the evolution of sexual decision making from microbes to humans. Princeton University Press, PrincetonCrossRefGoogle Scholar
  87. Ryan MJ, Causey BA (1989) Alternative mating behavior in the swordtails Xiphophorus nigrensis and Xiphophorus pygmaeus (Pisces: Poeciliidae). Behav Ecol Sociobiol 24(6):341–348Google Scholar
  88. Ryan MJ, Rosenthal GG (2001) Variation and selection in swordtails. In: Dugatkin LA (ed) Model systems in behavioral ecology. Princeton University Press, Princeton, pp 133–148Google Scholar
  89. Schlupp I, McKnab R, Ryan MJ (2001) Sexual harassment as a cost for molly females: bigger males cost less. Behaviour 138:277–286CrossRefGoogle Scholar
  90. Sherry DF, Forbes M, Khurgel M, Ivy GO (1993) Females have a larger hippocampus than males in the brood-parasitic brown-headed cowbird. Proc Nat Acad Sci USA 90:7839–7843CrossRefPubMedGoogle Scholar
  91. Smith CC (2007) Independent effects of male and female density on sexual harassment, female fitness and male competition for mates in the western mosquitofish Gambusia affinis. Behav Ecol Sociobiol 61:1349–1358CrossRefGoogle Scholar
  92. Smith CC, Sargent RC (2006) Female fitness declines with increasing female density but not male harassment in the western mosquitofish, Gambusia affinis. Anim Behav 71:401–407CrossRefGoogle Scholar
  93. Trivers R (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine Gruyter, New York, pp 136–179Google Scholar
  94. Wang S, Ramsey ME, Cummings ME (2014) Plasticity of the mate choice mind: evoking choice-like brain responses in coercive mating systems. Genes Brain Behav 13:365–375CrossRefPubMedGoogle Scholar
  95. Wang S, Cummings ME, Kirkpatrick M (2015) Coevolution of male courtship and sexual conflict characters in mosquitofish. Behav Ecol 26:1013–1020CrossRefGoogle Scholar
  96. Winge O (1937) Succession in broods of Lebistes reticulatus. Nature 140:467CrossRefGoogle Scholar
  97. Wong RY, Cummings ME (2014) Expression patterns of neuroligin-3 and tyrosine hydroxylase across the brain in mate choice contexts in female swordtails. Brain Behav Evol 83:231–243CrossRefPubMedGoogle Scholar
  98. Wong RY, So P, Cummings ME (2011) How female size and male displays influence mate preference in a swordtail. Anim Behav 82:691–697CrossRefGoogle Scholar
  99. Wong RY, Ramsey ME, Cummings ME (2012) Localizing brain regions associated with female mate preference behavior in a swordtail. PLoS One 7:e50355CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Integrative BiologyUniversity of TexasAustinUSA

Personalised recommendations