Negative frequency-dependent selection or alternative reproductive tactics: maintenance of female polymorphism in natural populations

BMC Evolutionary Biology

Thomas N Sherratt¹  Hans Van Gossum²  Jessica Bots²  Arne Iserbyt² 

[1] Department of Biology, Carleton University, 1125 Colonel By Drive, Ottawa, ON, K1S 5B6, Canada;Department of Biology, University of Antwerp, Evolutionary Ecology Group, Groenenborgerlaan 171, Antwerp, BE-2020, Belgium

关键词: Sexual conflict;    Quantity-quality trade-off;    Odonata;    Male harassment;    Fitness;    Colour polymorphism;    Alternative reproductive tactics;   

Others  :  1086943
DOI  :  10.1186/1471-2148-13-139

 received in 2012-11-14, accepted in 2013-06-28,  发布年份 2013

【 摘 要 】

Background

Sex-limited polymorphisms have long intrigued evolutionary biologists and have been the subject of long-standing debates. The coexistence of multiple male and/or female morphs is widely believed to be maintained through negative frequency-dependent selection imposed by social interactions. However, remarkably few empirical studies have evaluated how social interactions, morph frequencies and fitness parameters relate to one another under natural conditions. Here, we test two hypotheses proposed to explain the maintenance of a female polymorphism in a species with extreme geographical variation in morph frequencies. We first elucidate how fecundity traits of the morphs vary in relation to the frequencies and densities of males and female morphs in multiple sites over multiple years. Second, we evaluate whether the two female morphs differ in resource allocation among fecundity traits, indicating alternative tactics to maximize reproductive output.

Results

We present some of the first empirical evidence collected under natural conditions that egg number and clutch mass was higher in the rarer female morph. This morph-specific fecundity advantage gradually switched with the population morph frequency. Our results further indicate that all investigated fecundity traits are negatively affected by relative male density (i.e. operational sex ratio), which confirms male harassment as selective agent. Finally, we show a clear trade-off between qualitative (egg mass) and quantitative (egg number) fecundity traits. This trade-off, however, is not morph-specific.

Conclusion

Our reported frequency- and density-dependent fecundity patterns are consistent with the hypothesis that the polymorphism is driven by a conflict between sexes over optimal mating rate, with costly male sexual harassment driving negative frequency-dependent selection on morph fecundity.

【 授权许可】

   
2013 Iserbyt et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Roulin A: The evolution, maintenance and adaptive function of genetic colour polymorphism in birds. Biol Rev 2004, 79:815-848.
• [2]Gray SM, McKinnon JS: Linking color polymorphism maintenance and speciation. Trends Ecol Evol 2007, 22:71-79.
• [3]Forsman A, Ahnesjö J, Caesar S, Karlsson M: A model of ecological and evolutionary consequences of color polymorphism. Ecology 2008, 89:34-40.
• [4]Ayala FJ, Campbell CA: Frequency-dependent selection. Annu Rev Ecol Syst 1974, 5:115-138.
• [5]Hori M: Frequency-dependent natural selection in the handedness of scale-eating cichlid fish. Science 1993, 260:216-219.
• [6]Maynard Smith J: Evolutionary genetics. New York: Oxford University Press; 1998.
• [7]Takahashi Y, Yoshimura J, Morita S, Watanabe M: Negative frequency-dependent selection in female color polymorphism of a damselfly. Evolution 2010, 64:3620-3628.
• [8]Oliveira RF, Taborsky M, Brockmann HJ: Alternative reproductive tactics. Cambridge: Cambridge University Press; 2008.
• [9]Punzalan D, Rodd FH, Hughes KA: Perceptual processes and the maintenance of polymorphism through frequency-dependent predation. Evol Ecol 2005, 19:303-320.
• [10]Svensson EI, Abbott J, Hardling R: Female polymorphism, frequency dependence, and rapid evolutionary dynamics in natural populations. Am Nat 2005, 165:567-576.
• [11]Clarke B, Donald PO: Frequency-dependent selection. Heredity 1962, 19:201-206.
• [12]Sinervo B, Lively CM: The rock-paper-scissors game and the evolution of alternative male strategies. Nature 1996, 380:240-243.
• [13]Sinervo B, Calsbeek R: The developmental, physiological, neural, and genetical causes and consequences of frequency-dependent selection in the wild. Annu Rev Ecol Syst 2006, 37:581-610.
• [14]Calsbeek R, Bonvini L, Cox RM: Geographic variation, frequency-dependent selection, and the maintenance of a female-limited polymorphism. Evolution 2010, 64:116-125.
• [15]Sinervo B, Svensson E, Comendant T: Density cycles and an offspring quantity and quality game driven by natural selection. Nature 2000, 406:985-988.
• [16]Olendorf R, Rodd FH, Punzalan D, Houde AE, Hurt C, Reznick DN, Hughes KA: Frequency-dependent survival in natural guppy populations. Nature 2006, 441:633-636.
• [17]Bleay C, Comendant T, Sinervo B: An experimental test of frequency-dependent selection on male mating strategy in the field. Proc Roy Soc B 2007, 274:2019-2025.
• [18]Gross MR: Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol Evol 1996, 11:92-98.
• [19]Härdling R, Bergsten J: Nonrandom mating preserves intrasexual polymorphism and stops population differentiation in sexual conflict. Am Nat 2006, 167:401-409.
• [20]Kunte K: Female-limited mimetic polymorphism: a review of theories and a critique of sexual selection as balancing selection. Anim Behav 2009, 78:1029-1036.
• [21]Svensson EI, Abbott JK, Gosden TP, Coreau A: Female polymorphisms, sexual conflict and limits to speciation processes in animals. Evol Ecol 2009, 23:93-108.
• [22]Cook SE, Vernon JG, Bateson M, Guilford T: Mate choice in the polymorphic African swallowtail butterfly, Papilio dardanus: male-like females may avoid sexual harassment. Anim Behav 1994, 47:389-397.
• [23]Reinhardt K, Harney E, Naylor R, Gorb S, Siva-Jothy MT: Female-limited polymorphism in the copulatory organ of a traumatically inseminating insect. Am Nat 2007, 170:931-935.
• [24]Van Gossum H, Sherratt TN, Cordero-Rivera A: The evolution of sex-limited colour polymorphism. In Dragonflies: Model Organisms for Ecological and Evolutionary Research. Edited by Córdoba-Aguilar A. Oxford: Oxford University Press; 2008:219-229.
• [25]Clutton-Brock TH, Parker G a: Sexual coercion in animal societies. Anim Behav 1995, 49:1345-1365.
• [26]Watson PJ, Arnqvist G, Stallmann RR: Sexual conflict and the energetic costs of mating and mate choice in water striders. Am Nat 1998, 151:46-58.
• [27]Córdoba-Aguilar A: A female evolutionary response when survival is at risk : male harassment mediates early reallocation of resources to increase egg number and size. Behav Ecol Sociobiol 2009, 63:751-763.
• [28]Fincke OM: Polymorphic signals of harassed female odonates and the males that learn them support a novel frequency-dependent model. Anim Behav 2004, 67:833-845.
• [29]Robertson HM: Female dimorphism and mating behaviour in a damselfly, Ischnura ramburi: females mimicking males. Anim Behav 1985, 33:805-809.
• [30]Sherratt TN: The evolution of female-limited polymorphisms in damselflies: a signal detection model. Ecol Lett 2001, 4:22-29.
• [31]Gavrilets S, Waxman D: Sympatric speciation by sexual conflict. Proc Natl Acad Sci USA 2002, 99:10533-10538.
• [32]Van Gossum H, Stoks R, Matthysen E, Valck F, De Bruyn L: Male choice for female colour morphs in Ischnura elegans (Odonata, Coenagrionidae): testing the hypotheses. Anim Behav 1999, 57:1229-1232.
• [33]Gosden TP, Svensson EI: Density-dependent male mating harassment, female resistance, and male mimicry. Am Nat 2009, 173:709-721.
• [34]Ting JJ, Bots J, Pérez Jvostov F, Van Gossum H, Sherratt TN: Effects of extreme variation in female morph frequencies on the mating behaviour of male damselflies. Behav Ecol Sociobiol 2009, 64:225-236.
• [35]Le Galliard J-F, Fitze PS, Ferrière R, Clobert J: Sex ratio bias, male aggression, and population collapse in lizards. Proc Natl Acad Sci USA 2005, 102:18231-18236.
• [36]Kokko H, Rankin DJ: Lonely hearts or sex in the city? Density-dependent effects in mating systems. Philos Trans Roy Soc B 2006, 361:319-334.
• [37]Van Gossum H, Sherratt TN: A dynamical model of sexual harassment in damselflies and its implications for female-limited polymorphism. Ecol Model 2008, 210:212-220.
• [38]Vercken E, Massot M, Sinervo B, Clobert J: Colour variation and alternative reproductive strategies in females of the common lizard Lacerta vivipara. J Evol Biol 2007, 20:221-232.
• [39]Takahashi Y, Watanabe M: Morph-specific fecundity and egg size in the female-dimorphic damselfly Ischnura senegalensis. Zool Sci 2010, 27:325-329.
• [40]Iserbyt A, Van Gossum H, Stoks R: Biogeographical survey identifies consistent alternative physiological optima and a minor role for environmental drivers in maintaining a polymorphism. PLoS One 2012, 7:e32648.
• [41]Fincke OM, Jödicke R, Paulson DR, Schultz TD: The evolution and frequency of female color morphs in Holarctic Odonata: why are male-like females typically the minority? Int J Odonatol 2005, 8:183-212.
• [42]Sánchez-Guillén R a, Van Gossum H, Cordero Rivera a: Hybridization and the inheritance of female colour polymorphism in two ischnurid damselflies (Odonata: Coenagrionidae). Biol J Linn Soc 2005, 85:471-481.
• [43]Iserbyt A, Bots J, Ting J, Jvostov FP, Forbes MR, Sherratt TN, Van Gossum H: Multi-annual variation in female morph frequencies of the polymorphic damselfly, Nehalennia irene, at continental and regional scales. Anim Biol 2009, 59:313-326.
• [44]Gosden TP, Stoks R, Svensson EI: Range limits, large-scale biogeographic variation, and localized evolutionary dynamics in a polymorphic damselfly. Biol J Linn Soc 2011, 102:775-785.
• [45]Takahashi Y, Morita S, Yoshimura J, Watanabe M: A geographic cline induced by negative frequency-dependent selection A geographic cline induced by negative frequency-dependent selection. BMC Evol Biol 2011, 11:256.
• [46]Westfall MJ, May ML: Damselflies of North America. Gainesville: Scientific Publishers; 1996.
• [47]Forbes MRL, Richarson JML, Baker RL: Frequency of female morphs is related to an index of male density in the damselfly, Nehalennia irene (Hagen). Ecoscience 1995, 2:28-33.
• [48]Van Gossum H, Robb T, Forbes MR, Rasmussen L: Female-limited polymorphism in a widespread damselfly: morph frequencies, male density, and phenotypic similarity of andromorphs to males. Can J Zool 2008, 86:1131-1138.
• [49]Lam E: Damselflies of the Northeast. A Guide to the Species of Eastern Canada and the Northeastern United States. New York: Biodiversity Books; 2004.
• [50]Iserbyt A, Bots J, Van Dongen S, Ting JJ, Van Gossum H, Sherratt TN: Frequency-dependent variation in mimetic fidelity in an intraspecific mimicry system. Proc Roy Soc B 2011, 278:3116-3122.
• [51]Corbet PS: Dragonflies: Behaviour and Ecology of Odonata. Essex: Harley Books; 1999.
• [52]Takahashi Y, Watanabe M: Female reproductive success is affected by selective male harassment in the damselfly Ischnura senegalensis. Anim Behav 2010, 79:211-216.
• [53]Dubois B: Damselflies of the North Woods. Duluth: Kollath-Stensaas Publishing; 2005.
• [54]Van Gossum H, Beirinckx K, Forbes MR, Sherratt TN: Do current hypotheses explain continental and seasonal variation in female morph frequencies of the damselfly, Nehalennia irene? Biol J Linn Soc 2007, 90:501-508.
• [55]Bots J, De Bruyn L, Van Dongen S, Smolders R, Van Gossum H: Female polymorphism, condition differences, and variation in male harassment and ambient temperature. Biol J Linn Soc 2009, 97:545-554.
• [56]Xu M, Fincke OM: Tests of the harassment-reduction function and frequency-dependent maintenance of a female-specific color polymorphism in a damselfly. Behav Ecol Sociobiol 2011, 65:1215-1227.
• [57]Abramoff MD, Magelhaes PJ, Ram SJ: Image processing with ImageJ. Biophoton Int 2004, 11:36-42.
• [58]Honěk A: Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 1993, 66:483-492.
• [59]Lease HM, Wolf BO: Lipid content of terrestrial arthropods in relation to body size, phylogeny, ontogeny and sex. Physiol Entomol 2011, 36:29-38.
• [60]Wheeler D: The role of nourishment in oogenesis. Annu Rev Entomol 1996, 41:407-431.
• [61]Lessells CM, Boag PT: Unrepeatable repeatabilities: a common mistake. Auk 1987, 104:116-121.
• [62]Chown SL, Gaston KJ: Body size variation in insects: a macroecological perspective. Biol Rev 2010, 85:139-169.
• [63]Rankin DJ, Dieckmann U, Kokko H: Sexual conflict and the tragedy of the commons. Am Nat 2011, 177:780-791.
• [64]Rossi BH, Nonacs P, Pitts-Singer TL: Sexual harassment by males reduces female fecundity in the alfalfa leafcutting bee, Megachile rotundata. Anim Behav 2010, 79:165-171.
• [65]Cooper IA: Ecology of sexual dimorphism and clinal variation of coloration in a damselfly. Am Nat 2010, 176:566-572.
• [66]Iserbyt A, Bots J, Van Gossum H, Jordaens K: Did historical events shape current geographic variation in morph frequencies of a polymorphic damselfly? J Zool 2010, 282:256-265.
• [67]Sánchez-Guillén RA, Hansson B, Wellenreuther M, Svensson EI, Cordero-Rivera A: The influence of stochastic and selective forces in the population divergence of female colour polymorphism in damselflies of the genus Ischnura. Heredity 2011, 107:513-522.
• [68]Cordero Rivera A, Sánchez-Guillén RA: Male-like females of a damselfly are not preferred by males even if they are the majority morph. Anim Behav 2007, 74:247-252.
• [69]Van Gossum H, Bots J, Heusden JV, Hammers M, Huyghe K, Morehouse NI: Reflectance spectra and mating patterns support intraspecific mimicry in the colour polymorphic damselfly Ischnura elegans. Evol Ecol 2011, 25:139-154.
• [70]Abbott JK, Gosden TP: Correlated morphological and colour differences among females of the damselfly Ischnura elegans. Ecol Entomol 2009, 34:378-386.
• [71]Bots J, Breuker CJ, Van Kerkhove a, Van Dongen S, De Bruyn L, Van Gossum H: Variation in flight morphology in a female polymorphic damselfly: intraspecific, intrasexual, and seasonal differences. Can J Zool 2009, 87:86-94.
• [72]Sherratt TN: The evolution of imperfect mimicry. Behav Ecol 2002, 13:821-826.
• [73]Stoks R, Córdoba-Aguilar A: Evolutionary ecology of Odonata: a complex life cycle perspective. Ann Rev Entomol 2012, 57:249-265.
• [74]Anholt BR: Cannibalism and early instar survival in a larval damselfly. Oecologia 1994, 99:60-65.
• [75]Padeffke T, Suhling F: Temporal priority and intra-guild predation in temporary waters: an experimental study using Namibian desert dragonflies. Ecol Entomol 2003, 28:340-347.
• [76]Schenk K, Söndgerath D: Influence of egg size differences within egg clutches on larval parameters in nine libellulid species (Odonata). Ecol Entomol 2005, 30:456-463.
• [77]McPeek MA: Determination of species composition in the Enallagma damselfly assemblages of permanent lakes. Ecology 1990, 71:83-98.
• [78]Rollinson N, Hutchings JA: Environmental quality predicts optimal offspring size in the wild. Am Nat 2013. in press
• [79]Bots J: The maintenance of female colour polymorphism in a damselfly - PhD thesis. Antwerp: Universiteit Antwerpen; 2008.
• [80]Van Gossum H, Stoks R, De Bruyn L: Frequency-dependent male mate harassment and intra-specific variation in its avoidance by females of the damselfly Ischnura elegans. Behav Ecol Sociobiol 2001, 51:69-75.
• [81]Iserbyt A, Van Gossum H: Unexpected absence of behavioural differences between female damselfly colour morphs. Anim Behav 2009, 78:1463-1469.
• [82]Thompson DJ, Hassall C, Lowe CD, Watts PC: Field estimates of reproductive success in a model insect: behavioural surrogates are poor predictors of fitness. Ecol Lett 2011, 14:905-913.