Abstract
One possible mechanism for the (co-)evolution of seemingly novel male traits and female preferences for them is that males exploit pre-existing female biases, and livebearing fishes (Poeciliidae) have been at the forefront of this research for almost two decades. Here, using 13 poeciliid species from four different genera, we tested whether mustache-like rostral filaments found in males of some Mexican molly (Poecilia sphenops) populations could have evolved due to exploitation of a pre-existing female bias. While Mexican mollies were the only species with a significant female association preference for mustached males, we also did not find any species exhibiting significant aversion for mustached males; rather, variance in female preference scores was large throughout. For example, more than 25% of females spent twice as much time with the mustached male compared to the non-mustached male in most species, but even 31% of Mexican molly females spent more time near the non-mustached male. Hence, a comparison of the strength of preference was inconclusive. We discuss the possibility that the female preference of P. sphenops for mustached males could be due to a female pre-existing bias (sensu lato), even if population means were not significant for species other than P. sphenops. This highlights the importance of distinguishing between population means and individual preferences when interpreting mate choice, and thus, adds depth to the concept of mating preferences as a motor for evolutionary change.
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References
Andersson M (1994) Sexual selection. Princeton University Press
Andersen T, Bollerup K, Toft S, Bilde T (2008) Why do males of the spider Pisaura mirabilis wrap their nuptial gifts in silk: female preference or male control? Ethology 114:775–781
Aspbury AS, Basolo AL (2002) Repeatable female preferences, mating order and mating success in the poeciliid fish, Heterandria formosa. Behav Ecol Sociobiol 51:238–244
Avise JC, Trexler JC, Travis J, Nelson WS (1991) Poecilia mexicana is the recent female parent of the unisexual fish P. formosa. Evolution 45:1530–1533
Basolo AL (1990a) Female preference for a male sword length in the green swordtail, Xiphophorus helleri (Pisces: Poeciliidae). Anim Behav 40:332–338
Basolo AL (1990b) Female preference predates the evolution of the sword in swordtail fish. Science 250:808–810
Basolo AL (1995a) A further examination of a pre-existing bias favouring a sword in the genus Xiphophorus. Anim Behav 50:365–375
Basolo AL (1995b) Phylogenetic evidence for the role of a preexisting bias in sexual selection. Proc R Soc B 259:307–311
Basolo AL (2002) Congruence between the sexes in preexisting receiver responses. Behav Ecol 13:832–837
Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783
Bilde T, Tuni C, Elsayed R, Pekar S, Toft S (2007) Nuptial gifts of male spiders: sensory exploitation of the female's maternal care instinct or foraging motivation? Anim Behav 73:267–273
Breden F, Ptacek MB, Rashed M, Taphorn D, Figueiredo CA (1999) Molecular phylogeny of the live-bearing fish genus Poecilia (Cyprinodontiformes: Poeciliidae). Mol Phylogenet Evol 12:95–104
Brooks R (1996) Copying and the repeatability of mate choice. Behav Ecol Sociobiol 39:323–329
Brooks R (2002) Variation in female mate choice within guppy populations: population divergence, multiple ornaments and the maintenance of polymorphism. Genetica 116:343–358
Brooks R, Endler JA (2001) Female guppies agree to differ: phenotypic and genetic variation in mate-choice behavior and the consequences for sexual selection. Evolution 55:1644–1655
Darnell RM (1962) Fishes of the Rio Tamesi and related coastal lagoons in east-central Mexico. Publ Inst Marine Sci, Univ Texas 8:299–365
Darwin C (1871) The descent of man and selection in relation to sex. John Murray, London
Eakley AL, Houde AE (2004) Possible role of female discrimination against ‘redundant’ males in the evolution of colour pattern polymorphism in guppies. Proc R Soc B 271:S299–S301
Endler JA (1992) Signals, signal conditions, and the direction of evolution. Am Nat 139:125–153
Endler JA, Basolo AL (1998) Sensory ecology, receiver biases and sexual selection. Trends Ecol Evol 13:415–420
Godin J-GJ, Dugatkin LA (1995) Variability and repeatability of female mating preference in the guppy. Anim Behav 49:1427–1433
Godin J-GJ, Hair KPE (2009) Mate-choice copying in free-ranging Trinidadian guppies (Poecilia reticulata). Behaviour 146:1443–1461
Higgins LA, Waugaman RD (2004) Sexual selection and variation: a multivariate approach to species-specific calls and preferences. Anim Behav 68:1139–1153
Hrbek T, Seckinger J, Meyer A (2007) A phylogenetic and biogeographic perspective on the evolution of poeciliid fishes. Mol Phylogenet Evol 43:986–998
Jennions MD, Petrie M (1997) Variation in mate choice and mating preferences: a review of causes and consequences. Biol Rev 72:283–327
Kodric-Brown A, Nicoletto PF (1997) Repeatability of female choice in the guppy: response to live and videotaped males. Anim Behav 54:369–376
Kramer DL, Bryant MJ (1995) Intestine length in the fishes of a tropical stream: 2. Relationships to diet—the long and short of a convoluted issue. Environ Biol Fish 42:129–141
Lampert KP, Schartl M (2008) The origin and evolution of a unisexual hybrid: Poecilia formosa. Philos Trans R Soc B 363:2901–2909
Lampert KP, Fischer P, Schartl M (2009) MHC variability in the clonal Amazon molly, Poecilia formosa: is copy number less important than genotype? Mol Ecol 18:1124–1136
Landmann K, Parzefall J, Schlupp I (1999) A sexual preference in the Amazon molly, Poecilia formosa. Environ Biol Fish 56:325–331
Madden JR, Tanner K (2003) Preferences for coloured bower decorations can be explained in a nonsexual context. Anim Behav 65:1077–1083
Marler CA, Ryan MJ (1997) Origin and maintenance of a female mating preference. Evolution 51:1244–1248
Poschadel J, Plath M, Schlupp I (2009) Divergent female preference in a clonal fish. Acta Ethol 12:55–60
Ptacek MB, Breden F (1998) Phylogenetic relationships among the mollies (Poeciliidae: Poecilia: Mollienesia group) based on mitochondrial DNA sequences. J Fish Biol 53:64–81
Rios-Cardenas O, Morris MR (2011) Precopulatory sexual selection in poeciliid fishes. In: Evans J, Pilastro A, Schlupp I (eds) Ecology and Evolution of Poeciliid Fishes. University of Chicago Press, Chicago, IL
Rodd FH, Hughes KA, Grether GF, Baril CT (2002) A possible non-sexual origin of mate preference: are male guppies mimicking fruit? Proc R Soc B 269:475–481
Rogers SM, Vamosi SM (2010) Frozen F1's amidst a masterpiece of nature: new insights into the rare hybrid origin of gynogenesis in the Amazon molly (Poecilia formosa). Mol Ecol 19:5086–5089
Rosenthal GG, Evans CS (1998) Female preferences for swords in Xiphophorus helleri reflects a bias for large apparent size. Proc Natl Acad Sci USA 95:4431–4436
Rosenthal GG, Wagner WE Jr, Ryan MJ (2002) Secondary reduction of preference for the sword ornament in the pygmy swordtail Xiphophorus nigrensis (Pisces: Poeciliidae). Anim Behav 63:37–45
Ryan MJ (1985) The túngara frog: a study in sexual selection and communication. University of Chicago Press, Chicago, IL
Ryan MJ (1990) Sexual selection, sensory systems and sensory exploitation. Oxf Surv Evol Biol 7:157–195
Ryan MJ, Keddy-Hector A (1992) Directional patterns of female mate choice and the role of sensory biases. Am Nat 139:S4–S35
Ryan MJ, Rand AS (1993) Sexual selection and signal evolution—the ghost of biases past. Phil Trans R Soc B 340:187–195
Ryan MJ, Rand AS (1995) Female responses to ancestral advertisement calls in the túngara frog. Science 269:390–392
Ryan MJ, Rand AS (1999) Phylogenetic influence on mating call preference in female túngara frogs, Physalaemus pustulosus. Anim Behav 57:945–956
Ryan MJ, Fox JH, Wilczynski W, Rand AS (1990) Sexual selection for sensory exploitation in the frog Physalaemus pustulosus. Nature 343:66–67
Sakaluk SK (2000) Sensory exploitation as an evolutionary origin to nuptial food gifts in insects. Proc R Soc B 267:339–343
Schartl M, Wilde B, Schlupp I, Parzefall J (1995) Evolutionary origin of a parthenoform, the Amazon molly Poecilia formosa, on the basis of a molecular genealogy. Evolution 49:827–835
Schaschl H, Tobler M, Plath M, Penn DJ, Schlupp I (2008) Polymorphic MHC loci in an asexual fish, the amazon molly (Poecilidae formosa; Poeciliidae). Mol Ecol 17:5220–5230
Schlupp I (2005) The evolutionary ecology of gynogenesis. Annu Rev Ecol Evol Syst 36:399–417
Schlupp I, Riesch R (2011) Evolution of unisexual reproduction. In: Evans J, Pilastro A, Schlupp I (eds) Ecology and evolution of Poeciliid Fishes. University of Chicago Press, Chicago, IL
Schlupp I, Ryan MJ (1996) Mixed-species shoals and the maintenance of a sexual-asexual mating system in mollies. Anim Behav 52:885–890
Schlupp I, Riesch R, Tobler M, Plath M, Parzefall J, Schartl M (2010) A novel, sexually selected trait in poeciliid fishes: female preference for mustache-like, rostral filaments in male Poecilia sphenops. Behav Ecol Sociobiol 64:1849–1855
Schlupp I, Waschulewski M, Ryan MJ (1999) Female preferences for naturally occurring novel male traits. Behaviour 136:519–527
Schultz RJ, Miller RR (1971) Species of the Poecilia sphenops complex (Pisces: Poeciliidae) in Mexico. Copeia 1971:282–290
Shaw K (1995) Phylogenetic tests of the sensory exploitation model of sexual selection. Trends Ecol Evol 10:117–120
Stöck M, Lampert KP, Möller D, Schlupp I, Schartl M (2010) Monophyletic origin of multiple clonal lineages in an asexual fish (Poecilia formosa). Mol Ecol 19:5204–5215
Tobler M (2008) Divergence in trophic ecology characterizes colonization of extreme habitats. Biol J Linn Soc 95:517–528
Tobler M, Plath M, Burmeister H, Schlupp I (2006) Black spots and female mating preferences in a sexual/asexual mating complex (Poecilia, Poeciliidae, Teleostei). Behav Ecol Sociobiol 60:159–165
Van de Weerd HA, Van Loo PLP, Van Zutphen LFM, Koolhaas JM, Baumans V (1998) Strength of preference for nesting material as environmental enrichment for laboratory mice. Appl Anim Behav Sci 55:369–382
Vrijenhoek RC (1979) Factors affecting clonal diversity and coexistence. Am Zool 19:787–797
Walling CA, Royle NJ, Lindström J, Metcalfe NB (2010) Do female association preferences predict the likelihood of reproduction? Behav Ecol Sociobiol 64:541–548
Wilczynski W, Rand AS, Ryan MJ (2001) Evolution of calls and auditory tuning in the Physalaemus pustulosus species group. Brain Behav Evol 58:137–151
Winemiller KO (1993) Seasonality of reproduction by livebearing fishes in tropical rain-forest streams. Oecologia 95:266–276
Witte K, Klink KB (2005) No preexisting bias in sailfin molly females, Poecilia latipinna, for a sword in males. Behaviour 142:283–303
Witte K, Ueding K (2003) Sailfin molly females (Poecilia latipinna) copy the rejection of a male. Behav Ecol 14:389–395
Wong BBM, Rosenthal GG (2006) Female disdain for swords in a swordtail fish. Am Nat 167:136–140
Acknowledgments
We thank R. B. Langerhans for his introduction to Mesquite and helpful discussions, as well as D. McLennan, and an anonymous reviewer for comments that greatly helped to improve this manuscript. The Mexican Government and the Municipal of Tacotalpa kindly issued permits to collect fish. Financial support came from NSF (DEB-0743406; to I. S.), and DFG (Deutsche Forschungsgemeinschaft; PL 470/1–2; to M.P.).
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McCoy, E., Syska, N., Plath, M. et al. Mustached males in a tropical poeciliid fish: emerging female preference selects for a novel male trait. Behav Ecol Sociobiol 65, 1437–1445 (2011). https://doi.org/10.1007/s00265-011-1154-x
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DOI: https://doi.org/10.1007/s00265-011-1154-x