Mating advantage for rare males in wild guppy populations
Abstract
To understand the processes that maintain genetic diversity is a long-standing challenge in evolutionary biology, with implications for predicting disease resistance, response to environmental change, and population persistence. Simple population genetic models are not sufficient to explain the high levels of genetic diversity sometimes observed in ecologically important traits. In guppies (Poecilia reticulata), male colour pattern is both diverse and heritable, and is arguably one of the most extreme examples of morphological polymorphism known. Negative frequency-dependent selection (NFDS), a form of selection in which genotypes are favoured when they are rare, can potentially maintain such extensive polymorphism, but few experimental studies have confirmed its operation in nature. Here we use highly replicated experimental manipulations of natural populations to show that males with rare colour patterns have higher reproductive fitness, demonstrating NFDS mediated by sexual selection. Rare males acquired more mates and sired more offspring compared to common males and, as previously reported, had higher rates of survival. Orange colour, implicated in other studies of sexual selection in guppies, did predict male reproductive success, but only in one of three populations. These data support the hypothesis that NFDS maintains diversity in the colour patterns of male guppies through two selective agents, mates and predators. Similar field-based manipulations of genotype frequencies could provide a powerful approach to reveal the underlying ecological and behavioural mechanisms that maintain genetic and phenotypic diversity.
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Frequency-dependent sexual selection in favor of rare variants has been observed in vertebrates.
“Frequency-dependent sexual selection in favor of rare variants has been observed in vertebrates (55, 56), and such selection favoring rare pigmentation morphs could have driven alleles associated with lighter hair and eye colors to higher frequency.”
From Direct evidence for positive selection of skin, hair, and eye pigmentation in Europeans during the last 5,000 y (2014) · cites this paper as [55]
Cites
NIH Image to ImageJ: 25 years of image analysis
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012) · Nature Methods · doi:10.1038/nmeth.2089 · Cited by 64,638 · see citing works
Evolution and the theory of games
Smith, J. M. (1976) · Springer eBooks · doi:10.1007/978-1-4684-7862-4_22 · Cited by 7,369 · see citing works
Evolution and the Theory of Games
Smith, J. M. (1982) · Cambridge University Press eBooks · doi:10.1017/cbo9780511806292 · Cited by 6,918 · see citing works
Kalinowski, S. T., Taper, M. L., & MARSHALL, T. C. (2007) · Molecular Ecology · doi:10.1111/j.1365-294x.2007.03089.x · Cited by 5,240 · see citing works
THE GENETIC BASIS OF EVOLUTIONARY CHANGE
Felsenstein, J. (1975) · Evolution · doi:10.1111/j.1558-5646.1975.tb00851.x · Cited by 3,551 · see citing works
The Genetic Basis of Evolutionary Change.
Felsenstein, J., & Lewontin, R. C. (1975) · Evolution · doi:10.2307/2407274 · Cited by 1,384 · see citing works
A Predator’s View of Animal Color Patterns
Endler, J. A. (1978) · Evolutionary Biology · doi:10.1007/978-1-4615-6956-5_5 · Cited by 1,226 · see citing works
Sex, Color, and Mate Choice in Guppies
Houde, A. E. (1998) · Princeton University Press eBooks · doi:10.1515/9780691207261 · Cited by 958 · see citing works
Self-citationHow pathogens drive genetic diversity: MHC, mechanisms and misunderstandings
Spurgin, L. G., & Richardson, D. S. (2010) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2009.2084 · Cited by 747 · see citing works
Which evolutionary processes influence natural genetic variation for phenotypic traits?
Mitchell‐Olds, T., Willis, J. H., & Goldstein, D. B. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2207 · Cited by 520 · see citing works
Magurran, A. E. (2005) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198527855.001.0001 · Cited by 505 · see citing works
Ayala, F. J., & Campbell, C. A. (1974) · Annual Review of Ecology and Systematics · doi:10.1146/annurev.es.05.110174.000555 · Cited by 467 · see citing works
Reznick, D. N., Butler, M. J., Rodd, F. H., & Ross, P. N. (1996) · Evolution · doi:10.1111/j.1558-5646.1996.tb03937.x · Cited by 391 · see citing works
Self-citationGigord, L., Macnair, M. R., & Smithson, A. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.111162598 · Cited by 362 · see citing works
Equal mating success among male reproductive strategies in a marine isopod
Shuster, S. M., & Wade, M. J. (1991) · Nature · doi:10.1038/350608a0 · Cited by 350 · see citing works
Brooks, R. C., & Endler, J. A. (2001) · Evolution · doi:10.1554/0014-3820(2001)055[1002:daissa]2.0.co;2 · Cited by 277 · see citing works
Directional postcopulatory sexual selection revealed by artificial insemination
Evans, J. P., Zane, L., Francescato, S., & Pilastro, A. (2003) · Nature · doi:10.1038/nature01367 · Cited by 272 · see citing works
Familiarity leads to female mate preference for novel males in the guppy, Poecilia reticulata
Hughes, K. A., DU, L., Rodd, F. H., & Reznick, D. N. (1999) · Animal Behaviour · doi:10.1006/anbe.1999.1225 · Cited by 271 · see citing works
Self-citationFrequency-dependent survival in natural guppy populations
Olendorf, R., Rodd, F. H., Punzalan, D., Houde, A. E., Hurt, C. R., Reznick, D. N., & Hughes, K. A. (2006) · Nature · doi:10.1038/nature04646 · Cited by 250 · see citing works
Self-citationTurelli, M., & Barton, N. (2004) · Genetics · doi:10.1534/genetics.166.2.1053 · Cited by 244 · see citing works
Farr, J. A. (1977) · Evolution · doi:10.1111/j.1558-5646.1977.tb00993.x · Cited by 159 · see citing works
Rodriguez, R. N. (2010) · Wiley Interdisciplinary Reviews Computational Statistics · doi:10.1002/wics.131 · Cited by 154 · see citing works
Direct male-male competition can facilitate invasion of new colour types in Lake Victoria cichlids
Dijkstra, P. D., Seehausen, O., & Groothuis, T. G. G. (2005) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-005-0919-5 · Cited by 117 · see citing works
NEGATIVE FREQUENCY-DEPENDENT SELECTION IN FEMALE COLOR POLYMORPHISM OF A DAMSELFLY
Takahashi, Y., Yoshimura, J., Morita, S., & Watanabe, M. (2010) · Evolution · doi:10.1111/j.1558-5646.2010.01083.x · Cited by 98 · see citing works
Evolution of frequency-dependent mate choice: keeping up with fashion trends
Kokko, H., Jennions, M. D., & Houde, A. E. (2007) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2007.0043 · Cited by 84 · see citing works
Self-citationGenetic and environmental effects on secondary sex traits in guppies (Poecilia reticulata)
Hughes, K. A., Rodd, F. H., & Reznick, D. N. (2005) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2004.00806.x · Cited by 75 · see citing works
Self-citationEvans, J. P., Pilastro, A., & Ramnarine, I. W. (2003) · Biological Journal of the Linnean Society · doi:10.1046/j.0024-4066.2002.00193.x · Cited by 71 · see citing works
An experimental test of frequency-dependent selection on male mating strategy in the field
Bleay, C., Comendant, T., & Sinervo, B. (2007) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2007.0361 · Cited by 68 · see citing works
Zajitschek, S. R. K., & Brooks, R. C. (2008) · The American Naturalist · doi:10.1086/593001 · Cited by 68 · see citing works
Evidence for sperm transfer during sneaky mating in wild Trinidadian guppies
Matthews, I., & Magurran, A. E. (2000) · Journal of Fish Biology · doi:10.1111/j.1095-8649.2000.tb02150.x · Cited by 56 · see citing works
Pires, M. N., Arendt, J., & Reznick, D. N. (2010) · Biological Journal of the Linnean Society · doi:10.1111/j.1095-8312.2010.01391.x · Cited by 53 · see citing works
Johnson, A. M., Chappell, G. A., Price, A. C., Rodd, F. H., Olendorf, R., & Hughes, K. A. (2010) · Ethology · doi:10.1111/j.1439-0310.2010.01763.x · Cited by 46 · see citing works
Self-citationOBSERVATIONS ON REPRODUCTION OF THE POECILIID LEBISTES RETICULATUS (PETERS)
Rosenthal, H. L. (1952) · Biological Bulletin · doi:10.2307/1538621 · Cited by 44 · see citing works
Hampton, K. J., Hughes, K. A., & Houde, A. E. (2009) · Ethology · doi:10.1111/j.1439-0310.2009.01634.x · Cited by 38 · see citing works
Self-citationPrimers for 12 polymorphic microsatellite DNA loci from the guppy (Poecilia reticulata)
Olendorf, R., REUDI, B., & Hughes, K. A. (2004) · Molecular Ecology Notes · doi:10.1111/j.1471-8286.2004.00777.x · Cited by 18 · see citing works
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Wilde, S., Timpson, A., Kirsanow, K., Kaiser, E., Kayser, M., Unterländer, M., Hollfelder, N., Potekhina, I. D., Schier, W., Thomas, M. G., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1316513111 · Cited by 257 · see citing works
“Frequency-dependent sexual selection in favor of rare variants has been observed in vertebrates (55, 56), and such selection favoring rare pigmentation morphs could have driven alleles associated with lighter hair and eye colors to higher frequency.”
BackgroundRoulin, A. (2015) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12171 · Cited by 199 · see citing works
“This so-called ‘negative frequency-dependent selection’ has been demonstrated in the context of sexual selection, with males that display a rare colouration enjoying a mating advantage (Hughes et al., 2013).”
BackgroundSexual selection and genetic colour polymorphisms in animals
Wellenreuther, M., SVENSSON, E. I., & Hansson, B. (2014) · Molecular Ecology · doi:10.1111/mec.12935 · Cited by 185 · see citing works
“Extent of orange male spots is also a basis for female choice Linkage mapping and QTL analyses showed that most male colour traits are controlled by multiple genes, including genes on autosomes Hughes et al. (2013), Tezuka et al. (2011)”
BackgroundSheehan, M. J., & Nachman, M. W. (2014) · Nature Communications · doi:10.1038/ncomms5800 · Cited by 145 · see citing works
“Preferences for individuals with rare phenotypes have also been shown in other animals, such as guppies where rare phenotypes confer a survival advantage due to reduced predation 14,17 .”
InfluentialDing, B., Patterson, E. L., Holalu, S. V., Li, J., Johnson, G. A., Stanley, L. E., Greenlee, A. B., Peng, F., Bradshaw, H. D., Blinov, M. L., et al. (2020) · Current Biology · doi:10.1016/j.cub.2019.12.067 · Cited by 134 · see citing works
Advantageous diversity maintained by balancing selection in humans
Key, F. M., Teixeira, J. C., de Filippo, C., & Andrés, A. M. (2014) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2014.08.001 · Cited by 120 · see citing works
Polymorphism at a mimicry supergene maintained by opposing frequency-dependent selection pressures
Chouteau, M., Llaurens, V., Piron‐Prunier, F., & Joron, M. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1702482114 · Cited by 111 · see citing works
“However, sexual preferences may maintain color polymorphism through a preference for rare phenotypes (24) or from disassortative mating [i.”
BackgroundAn Evolutionary Perspective on Appearance Enhancement Behavior
Davis, A. C., & Arnocky, S. A. (2020) · Archives of Sexual Behavior · doi:10.1007/s10508-020-01745-4 · Cited by 111 · see citing works
Exaggerated heterochiasmy in a fish with sex-linked male coloration polymorphisms
Bergero, R., Gardner, J., Bader, B., Yong, L., & Charlesworth, D. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1818486116 · Cited by 102 · see citing works
“guppy populations, negative frequency-dependent selection also contributes to maintaining these SA polymorphisms, as rare male morphs have advantages in mating (25) and higher survival (21).”
BackgroundParichy, D. M., & Spiewak, J. E. (2014) · Pigment Cell & Melanoma Research · doi:10.1111/pcmr.12332 · Cited by 99 · see citing works
“…al., 2012; Greenwood et al., 2012; Kottler et al., 2014;Mills and Patterson, 2008; Seehausen et al., 2008), including the evolution of species-specific ornaments and other pigmentary adaptations (Hughes et al., 2013; Kemp et al., 2009; Kottler et al., 2014;Martin et al., 2014; Santos et al., 2014).”
BackgroundCorrelational selection in the age of genomics
SVENSSON, E. I., Arnold, S. J., Bürger, R., Csilléry, K., Draghi, J. A., Henshaw, J. M., Jones, A. G., Lisle, S. P. D., Marques, D. A., McGuigan, K., et al. (2021) · Nature Ecology & Evolution · doi:10.1038/s41559-021-01413-3 · Cited by 98 · see citing works
The Persistence of Polymorphisms across Species Radiations
Jamie, G. A., & Meier, J. I. (2020) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2020.04.007 · Cited by 91 · see citing works
The Genome of the Trinidadian Guppy, Poecilia reticulata, and Variation in the Guanapo Population
Künstner, A., Hoffmann, M., Fraser, B. A., Kottler, V. A., Sharma, E., Weigel, D., & Dreyer, C. (2016) · PLoS ONE · doi:10.1371/journal.pone.0169087 · Cited by 92 · see citing works
“Negative frequency dependent selection has been shown to be operating in guppies, where males with rare color patterns have a higher probability of surviving [24] and a higher mating advantage [25].”
BackgroundNegative frequency-dependent preferences and variation in male facial hair
Janif, Z. J., Brooks, R. C., & Dixson, B. J. W. (2014) · Biology Letters · doi:10.1098/rsbl.2013.0958 · Cited by 90 · see citing works
Female brain size affects the assessment of male attractiveness during mate choice
Corral‐López, A., Bloch, N. I., Kotrschal, A., van der Bijl, W., Buechel, S. D., Mank, J. E., & Kolm, N. (2017) · Science Advances · doi:10.1126/sciadv.1601990 · Cited by 79 · see citing works
Fitzpatrick, S. W., Gerberich, J. C., Angeloni, L. M., Bailey, L. L., Broder, E. D., Torres‐Dowdall, J., Handelsman, C. A., López‐Sepulcre, A., Reznick, D. N., Ghalambor, C. K., et al. (2016) · Evolutionary Applications · doi:10.1111/eva.12356 · Cited by 78 · see citing works
“Features of the guppy mating system such as female preference for novel male color patterns (Eakley and Houde 2004; Olendorf et al. 2006; Hughes et al. 2013) and forced copulation by males (Evans et al. 2003) limit the development of prezygotic reproductive barriers (Labonne and Hendry 2010).”
Sandkam, B. A., Young, C. M., & Breden, F. J. (2014) · Molecular Ecology · doi:10.1111/mec.13058 · Cited by 65 · see citing works
“mate preferences vary both within and between populations in response to environmental factors, making this system a premier model for evaluating the relative importance of the above models (Haskins et al. 1961; Endler 1980; Houde & Endler 1990; Brooks & Endler 2001; Hughes et al. 2013).”
BackgroundExperimental Studies of Evolution and Eco-Evo Dynamics in Guppies (Poecilia reticulata)
Reznick, D. N., & Travis, J. (2019) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev-ecolsys-110218-024926 · Cited by 63 · see citing works
Divergence and Remarkable Diversity of the Y Chromosome in Guppies
Almeida, P., Sandkam, B. A., Morris, J., Darolti, I., Breden, F. J., & Mank, J. E. (2020) · Molecular Biology and Evolution · doi:10.1093/molbev/msaa257 · Cited by 57 · see citing works
“1999), and several experimental studies suggest that rare male coloration polymorphisms could be maintained by sexual selection via negative frequency-dependent selection (Endler 1988; Olendorf et al. 2006; Hughes et al. 2013; Kemp et al. 2018).”
BackgroundSelection analysis on the rapid evolution of a secondary sexual trait
Gordon, S. P., Reznick, D. N., Arendt, J., Roughton, A., Hernandez, M. N. O., Bentzen, P., & López‐Sepulcre, A. (2015) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2015.1244 · Cited by 57 · see citing works
“Females also prefer males with unusual colour patterns, causing negative frequency-dependent selection, which enhances the diversity of male coloration [22,23].”
BackgroundSheehan, M. J., Lee, V., Corbett-Detig, R. B., Bi, K., Beynon, R. J., Hurst, J. L., & Nachman, M. W. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1005891 · Cited by 51 · see citing works
“In theory, a preference for novel MUP patterns could drive the evolution of extreme polymorphism as has been suggested to contribute to male color polymorphism in guppies [78,79].”
BackgroundMiles, M. C., Schuppe, E. R., Ligon, R. M., & Fuxjager, M. J. (2018) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2017.2628 · Cited by 55 · see citing works
“This idea that complex displays are shaped by multiple evolutionary forces was first supported by studies of Trinidadian guppies, where male ornamentation varying in both colour and pattern is shaped not only by sexual selection, but also local predation pressure and visibility [2,4].”
BackgroundTibbetts, E. A., Mullen, S. P., & Dale, J. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0347 · Cited by 50 · see citing works
Does gene flow aggravate or alleviate maladaptation to environmental stress in small populations?
Fitzpatrick, S. W., & Reid, B. N. (2019) · Evolutionary Applications · doi:10.1111/eva.12768 · Cited by 46 · see citing works
Improved Reference Genome Uncovers Novel Sex-Linked Regions in the Guppy (Poecilia reticulata)
Fraser, B. A., Whiting, J. R., Paris, J. R., Weadick, C. J., Parsons, P. J., Charlesworth, D., Bergero, R., Bemm, F., Hoffmann, M., Kottler, V. A., et al. (2020) · Genome Biology and Evolution · doi:10.1093/gbe/evaa187 · Cited by 45 · see citing works
Early neurogenomic response associated with variation in guppy female mate preference
Bloch, N. I., Corral‐López, A., Buechel, S. D., Kotrschal, A., Kolm, N., & Mank, J. E. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0682-4 · Cited by 39 · see citing works
Kottler, V. A., Koch, I., Floetenmeyer, M., Hashimoto, H., Weigel, D., & Dreyer, C. (2014) · PLoS ONE · doi:10.1371/journal.pone.0085647 · Cited by 43 · see citing works
“Studies have demonstrated that guppy females favor males with rare or novel color patterns over males with familiar phenotypes, suggesting that negative frequencydependent selection contributes to the maintenance of male color polymorphisms within guppy populations [19–23].”
BackgroundAdvancing mate choice studies in salmonids
Auld, H. L., Noakes, D. L. G., & Banks, M. A. (2019) · Reviews in Fish Biology and Fisheries · doi:10.1007/s11160-019-09551-5 · Cited by 42 · see citing works
Synergistic selection regimens drive the evolution of display complexity in birds of paradise
Miles, M. C., & Fuxjager, M. J. (2018) · Journal of Animal Ecology · doi:10.1111/1365-2656.12824 · Cited by 41 · see citing works
Gomes-Silva, G., Cyubahiro, E., Wronski, T., Riesch, R., Apio, A., & Plath, M. W. (2020) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2020.138912 · Cited by 41 · see citing works
Indirect Genetic Effects: A Cross-disciplinary Perspective on Empirical Studies
Baud, A., McPeek, S. J., Chen, N. X., & Hughes, K. A. (2021) · Journal of Heredity · doi:10.1093/jhered/esab059 · Cited by 44 · see citing works
Self-citationCharlesworth, D. (2018) · Genes · doi:10.3390/genes9050264 · Cited by 38 · see citing works
“The polymorphisms are not maintained solely by SA selection, but their maintenance is probably aided by being combined with advantages to rare male phenotypes during mating and under predation [46,47].”
BackgroundThreshold-Dependent Gene Drives in the Wild: Spread, Controllability, and Ecological Uncertainty
Backus, G. A., & Delborne, J. (2019) · BioScience · doi:10.1093/biosci/biz098 · Cited by 38 · see citing works
Kemp, D. J., Batistic, F., & Reznick, D. N. (2018) · Evolution · doi:10.1111/evo.13564 · Cited by 37 · see citing works
Technicolour deceit: a sensory basis for the study of colour-based lures
White, T. E., & Kemp, D. J. (2015) · Animal Behaviour · doi:10.1016/j.anbehav.2015.04.025 · Cited by 36 · see citing works
Johannesson, K., & Butlin, R. K. (2016) · Heredity · doi:10.1038/hdy.2016.77 · Cited by 35 · see citing works
“There is convincing experimental support for negative frequency-dependent selection of colour polymorphic prey species in some specific cases (Endler, 1980; Reid, 1987; Jormalainen et al., 1995; Olendorf et al., 2006; Hughes et al., 2013).”
BackgroundA Paradox of Genetic Variance in Epigamic Traits: Beyond “Good Genes” View of Sexual Selection
Radwan, J., Engqvist, L., & Reinhold, K. (2015) · Evolutionary Biology · doi:10.1007/s11692-015-9359-y · Cited by 34 · see citing works
“Based on this, the ‘‘genic capture’’ hypothesis posits that genetic variation in the expression of sexual traits represents genetic variation in resource acquisition and utilisation efficiency, or ‘‘condition’’ (Andersson 1986; Rowe and Houle 1996).”
BackgroundTwo ways to display: male hummingbirds show different color-display tactics based on sun orientation
Simpson, R. K., & McGraw, K. J. (2018) · Behavioral Ecology · doi:10.1093/beheco/ary016 · Cited by 33 · see citing works
“One potential explanation is that males transition between the 2 different display strategies to present females with a novel/different stimuli (i.e., negative frequencydependent mating advantage; Hughes et al. 2013).”
BackgroundFemale guppies can recognize kin but only avoid incest when previously mated
Daniel, M. J., & Rodd, F. H. (2015) · Behavioral Ecology · doi:10.1093/beheco/arv122 · Cited by 32 · see citing works
Self-citationDijkstra, P. D., & Border, S. E. (2018) · Current Zoology · doi:10.1093/cz/zox079 · Cited by 30 · see citing works
“Negative frequency-dependent survival and reproductive success has been demonstrated in a number of polymorphic species with divergent competitive phenotypes (Sinervo and Lively 1996; Sinervo and Calsbeek 2006; Bleay et al. 2007; Mappes et al. 2008; Mokkonen et al. 2011; Hughes et al. 2013), but we need more details o…”
BackgroundEarly social learning triggers neurogenomic expression changes in a swordtail fish
Cui, R., Delclós, P. J., Schumer, M. E., & Rosenthal, G. G. (2017) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2017.0701 · Cited by 27 · see citing works
Female preference for rare males is maintained by indirect selection in Trinidadian guppies
Potter, T., Arendt, J., Bassar, R. D., Watson, B., Bentzen, P., Travis, J., & Reznick, D. N. (2023) · Science · doi:10.1126/science.ade5671 · Cited by 27 · see citing works
Frequency‐dependent selection for rare genotypes promotes genetic diversity of a tropical palm
Browne, L., & Karubian, J. O. (2016) · Ecology Letters · doi:10.1111/ele.12692 · Cited by 26 · see citing works
Early social experience shapes female mate choice in guppies
Macario, A., Croft, D. P., Endler, J. A., & Darden, S. K. (2017) · Behavioral Ecology · doi:10.1093/beheco/arx043 · Cited by 26 · see citing works
The effects of familiarity and mating experience on mate choice in mosquitofish, Gambusia holbrooki
Vega‐Trejo, R., O’Dea, R. E., Jennions, M. D., & Head, M. L. (2014) · Behavioral Ecology · doi:10.1093/beheco/aru113 · Cited by 25 · see citing works
“This is consistent with a trend for female guppies to prefer males with phenotypes that they are unlikely to have encountered previously (“rare male effect,” see Zajitschek and Brooks 2008; Hughes et al. 2013).”
BackgroundDuVal, E. H., Fitzpatrick, C. L., Hobson, E. A., & Servedio, M. R. (2023) · PLoS Biology · doi:10.1371/journal.pbio.3002269 · Cited by 24 · see citing works
Mate Preference for Novel Phenotypes: A Fresh Face Matters
Graber, R. E., Senagolage, M., Ross, E., Houde, A. E., & Hughes, K. A. (2014) · Ethology · doi:10.1111/eth.12313 · Cited by 24 · see citing works
Self-citationMeasuring frequency-dependent selection in culture
Newberry, M., & Plotkin, J. (2021) · Nature Human Behaviour · doi:10.1038/s41562-022-01342-6 · Cited by 24 · see citing works
Habituation underpins preference for mates with novel phenotypes in the guppy
Daniel, M. J., Koffinas, L., & Hughes, K. A. (2019) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2019.0435 · Cited by 23 · see citing works
Self-citationGotanda, K. M., & Hendry, A. P. (2014) · Biological Journal of the Linnean Society · doi:10.1111/bij.12261 · Cited by 22 · see citing works
“However, the reasons why females from this site might prefer an anomalous colour pattern are not known, although the initial impetus could be female preferences for novel males (Hughes et al., 2013).”
BackgroundStephenson, J. F., Stevens, M., Troscianko, J. T., & Jokela, J. (2020) · The American Naturalist · doi:10.1086/711033 · Cited by 22 · see citing works
“Furthermore, color pattern novelty confers higher reproductive fitness (Hughes et al. 2013) and some defense against predators (Olendorf et al. 2006) in natural conditions.”
BackgroundHeckley, A. M., Pearce, A. E., Gotanda, K. M., Hendry, A. P., & Oke, K. B. (2022) · Journal of Evolutionary Biology · doi:10.1111/jeb.14086 · Cited by 22 · see citing works
“The colour patterns that are most attractive to females and the least conspicuous to predators also can vary through time at a given site due to negative frequency dependent selection (Hughes et al., 2013; Olendorf et al., 2006).”
BackgroundVenables, S. K., Marshall, A. D., Germanov, E. S., Perryman, R. J. Y., Tapilatu, R. F., Hendrawan, I. G., Flam, A. L., van Keulen, M., Tomkins, J. L., & Kennington, W. J. (2019) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2019.1879 · Cited by 22 · see citing works
Burns, J. G., Price, A. C., Thomson, J. D., Hughes, K. A., & Rodd, F. H. (2016) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-016-2127-x · Cited by 22 · see citing works
“types have higher mating success (Hughes et al. 2013).”
BackgroundSelf-citationConsistent female preference for rare and unfamiliar male color patterns in wild guppy populations
Valvo, J. J., Rodd, F. H., & Hughes, K. A. (2019) · Behavioral Ecology · doi:10.1093/beheco/arz134 · Cited by 21 · see citing works
Self-citationUsing Delaunay triangulation to sample whole‐specimen color from digital images
Valvo, J. J., Aponte, J. D., Daniel, M. J., Dwinell, K., Rodd, H., Houle, D., & Hughes, K. A. (2021) · Ecology and Evolution · doi:10.1002/ece3.7992 · Cited by 21 · see citing works
“…in male guppy color patterns have been investigated extensively (e.g., Brooks, 2002; Brooks & Endler, 2001; Farr, 1977; Houde & Endler, 1990; Hughes et al., 1999, 2013), and based on this literature, we predicted that low-predation sites should exhibit more phenotype variation than…”
BackgroundSelf-citationEstévez, D. A. G., Kozminsky, E. V., Carvajal‐Rodríguez, A., Caballero, A., Faria, R., Galindo, J., & Rolán‐Alvarez, E. (2020) · Frontiers in Marine Science · doi:10.3389/fmars.2020.614237 · Cited by 21 · see citing works
Effects of methylphenidate on responses to novelty in a teleost fish (Poecilia reticulata)
Serrano, A. R. D., Fong, C., & Rodd, F. H. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.01.021 · Cited by 19 · see citing works
Self-citationHeterozygote advantage and pleiotropy contribute to intraspecific color trait variability
Pasqual, C. D., Suisto, K., Kirvesoja, J., Gordon, S. P., Ketola, T., & Mappes, J. (2022) · Evolution · doi:10.1111/evo.14597 · Cited by 19 · see citing works
“for example, through alternative male reproductive strategies in the side-blotched lizards (Uta stansburiana) (Sinervo and Lively 1996), through rare morph advantage in guppies (Poecilia reticulata) (Hughes et al., 2013), or through FD sexually antagonistic selection in blue-tailed damselflies (Ischnura elegans) (Sven…”
BackgroundPervasive indirect genetic effects on behavioral development in polymorphic eastern mosquitofish
Kraft, B., Lemakos, V. A., Travis, J., & Hughes, K. A. (2017) · Behavioral Ecology · doi:10.1093/beheco/arx180 · Cited by 19 · see citing works
Self-citationGangoso, L., & Figuerola, J. (2019) · Behavioral Ecology · doi:10.1093/beheco/arz013 · Cited by 19 · see citing works
“Nonetheless, these authors argue that detecting negative frequency-dependent selection under natural conditions is difficult, largely because the equilibrium frequencies of different morphs under this type of selection are those at which fitnesses are equal (Hughes et al. 2013).”
Visible Implant Elastomer tagging influences social preferences of zebrafish (Danio rerio)
Frommen, J. G., Hanak, S., Schmidl, C. A., & Thünken, T. (2015) · Behaviour · doi:10.1163/1568539x-00003303 · Cited by 19 · see citing works
“A potential reason for this might be that novel colour patterns might increase the attractiveness of the tagged fish as mating partners (Farr, 1977; Hughes et al., 2014).”
BackgroundYong, L., Croft, D. P., Troscianko, J. T., Ramnarine, I. W., & Wilson, A. J. (2021) · Molecular Ecology · doi:10.1111/mec.16039 · Cited by 18 · see citing works
Metabolism, oxidative stress and territorial behaviour in a female colour polymorphic cichlid fish
Dijkstra, P. D., Pierotti, M. E. R., D, O. S. C., & Metcalfe, N. B. (2015) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-015-2028-4 · Cited by 18 · see citing works
“mate choice, male-male or female-female conflict), predation risk and thermoregulation (Endler 1980; Majerus 1998; Bittner et al. 2002; Seehausen and Schluter 2004; Grether et al. 2009; Hughes et al. 2013).”
Sex-biased expression between guppies varying in the presence of ornamental coloration
Dick, C. A., Reznick, D. N., & Hayashi, C. Y. (2018) · PeerJ · doi:10.7717/peerj.5782 · Cited by 17 · see citing works
Paris, J. R., Whiting, J. R., Daniel, M. J., Ferrer, J., Parsons, P. J., van der Zee, M. J., Wheat, C. W., Hughes, K. A., & Fraser, B. A. (2022) · Nature Communications · doi:10.1038/s41467-022-28895-4 · Cited by 17 · see citing works
Self-citationTan, C. K. W., Doyle, P., Bagshaw, E., Richardson, D. S., Wigby, S., & Pizzari, T. (2016) · Evolution · doi:10.1111/evo.13145 · Cited by 17 · see citing works
Serrano, A. R. D., Hughes, K. A., & Rodd, F. H. (2021) · Scientific Reports · doi:10.1038/s41598-021-83448-x · Cited by 17 · see citing works
Self-citationPartial sex linkage and linkage disequilibrium on the guppy sex chromosome
Qiu, S., Yong, L., Wilson, A. J., Croft, D. P., Graham, C., & Charlesworth, D. (2022) · Molecular Ecology · doi:10.1111/mec.16674 · Cited by 17 · see citing works
Culumber, Z. W., Schumer, M. E., Monks, S., & Tobler, M. (2014) · Evolution · doi:10.1111/evo.12574 · Cited by 15 · see citing works
“For example, color polymorphisms in male guppies are maintained by negative frequency-dependent selection mediated by female mate choice (Hughes et al. 2013) and a survival advantage of rare males (Olendorf et al. 2006).”
BackgroundAre Preferences for Women’s Hair Color Frequency-Dependent?
Janif, Z. J., Brooks, R. C., & Dixson, B. J. W. (2014) · Adaptive Human Behavior and Physiology · doi:10.1007/s40750-014-0008-y · Cited by 16 · see citing works
“Males bearing rare colour patterns have greater survivability in the wild (Olendorf et al. 2006) and greater mating success in the lab (Farr 1977; Hughes et al. 1999) and the wild (Hughes et al. 2013).”
BackgroundColor polymorphism in an aphid is maintained by attending ants
Watanabe, S., Murakami, T., Yoshimura, J., & Hasegawa, E. (2016) · Science Advances · doi:10.1126/sciadv.1600606 · Cited by 16 · see citing works
“Negative frequency (or density) – dependent selection on various morphs is a prime example of this condition ( 4 – 8 ).”
Kin Recognition in Guppies Uses Self-Referencing Based on Olfactory Cues
Daniel, M. J., & Rodd, F. H. (2020) · The American Naturalist · doi:10.1086/712352 · Cited by 16 · see citing works
Self-citationColoration, Paternity, and Assortative Mating in Western Bluebirds
Jacobs, A. C., Fair, J. M., & Zuk, M. (2014) · Ethology · doi:10.1111/eth.12327 · Cited by 16 · see citing works
Westrick, S. E., Broder, E. D., Reznick, D. N., Ghalambor, C. K., & Angeloni, L. M. (2019) · Ethology · doi:10.1111/eth.12849 · Cited by 15 · see citing works
Prazdnikov, D. V. (2021) · Environmental Biology of Fishes · doi:10.1007/s10641-021-01102-x · Cited by 14 · see citing works
Frequency-Dependent Selection on Female Morphs Driven by Premating Interactions with Males
Bots, J., Iserbyt, A., GOSSUM, H. V., Hammers, M., & Sherratt, T. N. (2015) · The American Naturalist · doi:10.1086/681005 · Cited by 14 · see citing works
Exploratory behaviour covaries with preference for unfamiliar males in female guppies
Lucon‐Xiccato, T., Bisazza, A., & Pilastro, A. (2019) · Animal Behaviour · doi:10.1016/j.anbehav.2019.07.009 · Cited by 14 · see citing works
Bolder guppies do not have more mating partners, yet sire more offspring
Herdegen‐Radwan, M. (2019) · BMC Evolutionary Biology · doi:10.1186/s12862-019-1539-4 · Cited by 14 · see citing works
High-resolution characterization of male ornamentation and re-evaluation of sex linkage in guppies
Morris, J., Darolti, I., van der Bijl, W., & Mank, J. E. (2020) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2020.1677 · Cited by 14 · see citing works
Deep learning reveals the complex genetic architecture of male guppy colouration
van der Bijl, W., Shu, J. J., Goberdhan, V. S., Sherin, L. M., Jia, C., Cortázar‐Chinarro, M., Corral‐López, A., & Mank, J. E. (2025) · Nature Ecology & Evolution · doi:10.1038/s41559-025-02781-w · Cited by 13 · see citing works
“…female mate preference for rare male patterns probably acts to preserve some variation from the eroding forces of genetic drift and selection 5,13,14 , the genetic architecture underlying the extraordinary diversity in male guppy colour remains mysterious, as does the maintenance of this…”
Mating Preference for Novel Phenotypes Can Be Explained by General Neophilia in Female Guppies
Daniel, M. J., Koffinas, L., & Hughes, K. A. (2020) · The American Naturalist · doi:10.1086/710177 · Cited by 13 · see citing works
Self-citationVariation in Melanism and Female Preference in Proximate but Ecologically Distinct Environments
Culumber, Z. W., Bautista-Hernández, C. E., Monks, S., Arias‐Rodríguez, L., & Tobler, M. (2014) · Ethology · doi:10.1111/eth.12282 · Cited by 13 · see citing works
“Examples include plumage characteristics in birds (Hill 1990; Jawor et al. 2003), color polymorphic lizards (Perez i de Lanuza et al. 2013), and coloration in fish (Seehausen & van Alphen 1998; Kingston et al. 2003; Takahashi & Hori 2008; Hughes et al. 2013).”
BackgroundEffect of induced mutations on sexually selected traits in the guppy, Poecilia reticulata
Herdegen‐Radwan, M., & Radwan, J. (2015) · Animal Behaviour · doi:10.1016/j.anbehav.2015.09.013 · Cited by 13 · see citing works
Katsumura, T., Oda, S., Nakagome, S., Hanihara, T., Kataoka, H., Mitani, H., Kawamura, S., & Oota, H. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2014.2259 · Cited by 13 · see citing works
“Although recent studies have indicated which evolutionary mechanism explains empirical phenotypic variation [11,12], the exact mechanism by which related genes influence the variation remains unknown.”
BackgroundHow to generate and test hypotheses about colour: insights from half a century of guppy research
Kemp, D. J., Reznick, D. N., Arendt, J., van den Berg, C. P., & Endler, J. A. (2023) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2022.2492 · Cited by 12 · see citing works
Meta‐analytical evidence for frequency‐dependent selection across the tree of life
Gómez‐Llano, M., Bassar, R. D., SVENSSON, E. I., Tye, S. P., & Siepielski, A. M. (2024) · Ecology Letters · doi:10.1111/ele.14477 · Cited by 12 · see citing works
Řežucha, R., & Reichard, M. (2014) · Journal of Evolutionary Biology · doi:10.1111/jeb.12567 · Cited by 12 · see citing works
Ruberto, T., Clément, R. J. G., Spinello, C., Neri, D., Macrı̀, S., & Porfiri, M. (2018) · Zebrafish · doi:10.1089/zeb.2018.1616 · Cited by 10 · see citing works
“60,61 It is still unclear whether the increases in activity and social interactions within the groups reflect attraction, repulsion, or another type of response be-tween the tagged and the nontagged fish.”
Herdegen‐Radwan, M., Cattelan, S., Buda, J., Raubic, J., & Radwan, J. (2021) · Evolution · doi:10.1111/evo.14384 · Cited by 11 · see citing works
“Furthermore, guppies are an established model system for studying the evolution of male ornaments and female mating preferences (Endler 1980; Houde 1997; Magurran 2005; Hughes et al. 2013).”
BackgroundMould, M. C., Huet, M., Senegas, L., Milá, B., Thébaud, C., Bourgeois, Y., & Chaine, A. S. (2022) · Journal of Evolutionary Biology · doi:10.1111/jeb.14124 · Cited by 10 · see citing works
“Frequency dependent selection could also favour the coexistence of multiple colour variants, if rare variants are at an advantage with regards to predator avoidance (Torres-Dowdall et al., 2017) or sexual and social selection (Dijkstra et al., 2010; Hughes et al., 2013).”
Martínez, C., Chavarría, C., Sharpe, D. M. T., & León, L. F. D. (2016) · PLoS ONE · doi:10.1371/journal.pone.0148040 · Cited by 10 · see citing works
“In contrast, maintenance of high variability in the less abundant colours is consistent with the role of negativefrequency selection by females for rare colour patterns [14,63,72,73].”
BackgroundResultLiebherr, J. K., & Will, K. (2015) · Insect Systematics & Evolution · doi:10.1163/1876312x-45042124 · Cited by 10 · see citing works
“Such a situation would result in negative frequency-dependent selection (Hughes et al. 2013), and for chiral antisymmetry, left-right male ratios would hover near 1:1; a condition termed pure antisymmetry (Schilthuizen 2013).”
BackgroundThe developmental and genetic trajectory of coloration in the guppy (Poecilia reticulata)
Dick, C. A., Arendt, J., Reznick, D. N., & Hayashi, C. Y. (2018) · Evolution & Development · doi:10.1111/ede.12268 · Cited by 10 · see citing works
“The more rare of two color types (either colored or uncolored caudal fins) has higher short-term survival (Olendorf et al., 2006) and reproductive success (Hughes et al., 2013) than the more common type.”
BackgroundMales optimally balance selfish and kin-selected strategies of sexual competition in the guppy
Daniel, M. J., & Williamson, R. J. (2020) · Nature Ecology & Evolution · doi:10.1038/s41559-020-1152-3 · Cited by 9 · see citing works
Olfactory receptor OR52N2 for PGE2 in mediation of guppy courtship behaviors
Jing, X., Lyu, L., Gong, Y., Wen, H., Li, Y., Wang, X., Li, J., Yao, Y., Zuo, C., Xie, S., et al. (2023) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2023.124518 · Cited by 9 · see citing works
Swierk, L., Boyer, J. F. F., Chang, J., Petelo, M., & Drobniak, S. M. (2020) · Evolutionary Ecology · doi:10.1007/s10682-020-10085-7 · Cited by 9 · see citing works
Laplace's demon in biology: Models of evolutionary prediction
Gompert, Z., Flaxman, S. M., Feder, J. L., Chevin, L., & Nosil, P. (2022) · Evolution · doi:10.1111/evo.14628 · Cited by 9 · see citing works
“This has been documented, for example, in cichlids, guppies, stickleback, and stick insects (Hori, 1993; Olendorf et al., 2006; Hughes et al., 2013; Bolnick & Stutz, 2017; Nosil et al., 2018).”
BackgroundYoshikawa, T., Ohkubo, Y., Karino, K., & Hasegawa, E. (2016) · Animal Behaviour · doi:10.1016/j.anbehav.2016.05.022 · Cited by 9 · see citing works
“Together with the rare-male mating advantage (Hughes et al., 2013) and high predation risk for commonmale phenotypes (Olendorf et al., 2006), our results will shed light on themechanism for themaintenance of male ornamentation.”
BackgroundBorges, I. L., Dangerfield, J. C., Angeloni, L. M., Funk, W. C., & Fitzpatrick, S. W. (2021) · Ecology Letters · doi:10.1111/ele.13929 · Cited by 8 · see citing works
- Authors
- Hughes, K. A., Houde, A. E., Price, A. C., & Rodd, F. H.
- Affiliations
- Florida State University (US)
- Lake Forest College (US)
- University of Toronto (CA)
- Corresponding author
- Hughes, Kimberly A.
- Venue
- Nature
- Published
- 2013-10-30
- Volume
- 503
- Issue
- 7474
- Pages
- 108-110
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W1979821803
- Cited by
- 169
- References
- 34
- Citations by year
- 2026: 9 · 2025: 2 · 2024: 3 · 2023: 12 · 2022: 10 · 2021: 13 · 2020: 18 · 2019: 18 · 2018: 16 · 2017: 13 · 2016: 17 · 2015: 13 · 2014: 24 · 2013: 1
- FWCI
- 19.49
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Evolutionary Psychology and Human Behavior
- Keywords
- Poecilia reticulata, negative frequency-dependent selection, sexual selection, reproductive success, maintenance of genetic variation, female mate choice, predator avoidance, natural populations
- MeSH terms
- Animals, Animals, Wild, Female, Fertility, Male, Phenotype, Pigmentation, Poecilia, Predatory Behavior, Selection, Genetic, Genetic Variation, Survival Rate, Models, Animal, Rivers, Mating Preference, Animal, Genetic Fitness
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