The relationship between sexual selection and speciation

Current Zoology Editorial The relationship between sexual selection and speciation Maria R. SERVEDIO Department of Biology, University of North Carolina, Chapel Hill, NC 27599 USA, servedio@email.unc.edu 1 Introduction 2 Contributions to This Issue The articles in this column gather a fresh perspective on the role of sexual selection and speciation, from a variety of different angles. Interestingly, the bulk of the evidence from this column does not support a strong driving role for sexual selection in speciation, although a supportive role is provided by some of the studies. The Downloaded from https://academic.oup.com/cz/article/58/3/413/1816140 by guest on 13 November 2023 The intriguing relationship between sexual selection and speciation has sparked an increasing number of papers in recent years that have attempted to draw connections between the two processes. These include a myriad of theoretical and empirical studies, as well as several influential reviews (e.g. Price, 1998; Panhuis et al., 2001, Kirkpatrick and Ravigné, 2002; Ritchie, 2007; Maan and Seehausen, 2011). In particular, many researchers have speculated on whether sexual selection can lead to speciation, either alone, or in conjunction with ecological processes. Such speculation is tempting in part because of the obvious differences in secondary sexual characters that often exist between closely related species. Indeed one of the earliest and most influential of all sexual selection models, Lande’s (1981) paper “Models of speciation by sexual selection on a polygenic trait” centered its title on the role that sexual selection may play in speciation. What, however, is the evidence of a causal relationship between sexual selection and speciation? It turns out to be surprisingly ambiguous. Many have attempted to address a relationship by comparative studies, a process that can be problematic because of both methodological concerns and the fact that the presence of sexual selection is inferred by proxy (Kraaijeveld et al., 2011). Kraaijeveld et al. (2011) point out that these studies only sometimes support a correlation between sexual selection and speciation, and using a meta–analysis find only weak support for a relationship across multiple datasets. A large number of individual experimental studies have also examined various aspects of the intersection of sexual selection and speciation, but it is often unclear what would constitute a true test of the role of sexual selection in speciation, and unambiguous tests of this role are essentially absent (large scale literature analysis by Safran, Mendelson, Scordato and Symes, unpublished data). In particular, the relative roles of ecological factors and sexual selection often appear very intertwined and difficult to tease apart (case studies reviewed in Ritchie, 2007; Maan and Seehausen, 2011). Some studies have attempted to assess whether there is a difference between mate choice and species recognition (e.g. Kozak et al., 2009), but these have also found mixed results. Theoretical studies, which focus on the case of speciation with gene flow in particular, have also demonstrated a very mixed relationship between sexual selection and speciation. Many studies examining the evolution of premating isolation couch the language in terms of sexual selection, simply assuming that species recognition and sexual selection are one and the same in this regard. While this is strictly accurate by the definition of sexual selection as differential mating success, it does not address the spirit of the question of whether sexual selection processes within a species are ultimately responsible for speciation. Several theoretical studies have focused on whether sexual selection alone could account for sympatric speciation, but the general conclusion is that this is unlikely (e.g., van Doorn et al., 2004). Intriguingly, the theoretical literature has also in recent years developed an idea largely absent from the empirical literature, namely that the role of sexual selection in speciation with gene flow may often be inhibitory rather than driving (see discussion in Servedio and Kopp, 2012, this issue). Specifically, sexual selection may often eliminate variation necessary for speciation (e.g., Kirkpatrick and Nuismer, 2004), or lead to stabilizing selection that can counter divergent ecological selection to prevent speciation with gene flow (e.g., Matessi et al., 2001; Otto et al., 2008; Pennings et al., 2008). 414 Current Zoology No. 3 female Hawaiian crickets Laupaula cerasina are capable of discriminating very fine differences in pulse rate, on the order of the differences that males of these same populations show in the pulse rates of their song. Furthermore they find that the mean pulse rate preferred by females shows a tight correlation with the mean pulse rate sung in each population by males, and both preference and trait are heritable. These lines of evidence suggest that the small differences in song found between populations may serve as the basis of reproductive isolation, generated by sexual selection, between them. Two of the studies in the column tackle the interesting question of the relationship between sexual selection within a population and processes that discriminate between species. Pauers and McKinnon (2012), find that females may shift the cues that they use to discriminate between males depending on whether the context is within or between populations. Specifically, using populations of the fish Labeotropheus fuelleborni, they show that while females of a given population seem to use consistent rules for color preferences when comparing males from within a single population (either from the female’s population or from a different population), they deviate from this rule when asked to discriminate between two very different males, one from each population. Bolnick and Kirkpatrick (2012) instead ask whether the strength of assortative mating within species for a single trait can be extrapolated to account for levels of reproductive isolation between species, given the difference between them in this same trait. They find that such levels of assortative mating are not sufficient to account for isolation. This implies either that females (or males) indeed use different traits to discriminate within and between species, or that discrimination is based on a multivariate assortment of traits. The column ends with two syntheses. In an interesting twist to the topic, Qvarnström et al. (2012) point out that although current work on sexual selection and speciation almost universally focuses on sexual selection generated by female choice, there are likely to be a number of interesting ways in which male contest competition may promote speciation, including by generating disruptive selection and speeding adaptation in isolated or partially isolated populations. This review provides fodder for a shift to a novel focus in analyses of the ways in which sexual selection and speciation can be related. Finally, in an opinion piece, Servedio and Kopp (2012) suggest that a classification based upon “magic traits” may provide a way to answer the question of how often sexual selection is involved in speci- Downloaded from https://academic.oup.com/cz/article/58/3/413/1816140 by guest on 13 November 2023 papers in this collection also highlight some of the many difficulties inherent in addressing what the role of sexual selection in speciation may be. Two of the papers in this column find a lack of support for a correlation between sexual dimorphism, often used as a proxy for sexual selection, and reproductive isolation. In the first of these, Macías Garcia et al (2012) find that although exaggerated male fins in the Mexican freshwater fish Girardinichthys multiradiatus are preferred by females and evolve more quickly than female morphology, the amount of sexual dimorphism is negatively, not positively, correlated with assortative mating in laboratory tests. In a comparative study, Pfennig and Hurlbert (2012) examine the relationship between sexually dimorphic traits, presumably used in mate attraction, and the number of congeners found to coexist geographically. They find no relationship between the two in the majority of the bird families examined, suggesting that the number of sexually dimorphic traits may not reflect the ability of species to become or remain reproductively isolated when in contact with closely related species. Among other explanations, this result could indicate either that sexual selection does not strongly promote speciation in these groups, or that sexual dimorphism of the traits examined is not a sufficient proxy for sexual selection in these taxa (although dichromatic characters, which form the bulk of those used in this study, were found to have the largest effect size in Kraaijeveld et al. 2011). A third study also does not support an association between sexual selection and speciation. Rolán–Alvarez et al. (2012) find that shell color in the marine intertidal snail Littorina fabalis is under sexual selection, but serves as the basis of consistent disassortative, not assortative, mating. In this instance, therefore, the sexually selected trait would tend to cause population cohesion, rather than divergence. In contrast, evidence consistent with a correlation between sexual selection and speciation is also present in several of the studies in the column. Safran et al (2012), in a paper that introduces a new phenotypic distance measure with which to address such questions, find that among closely related populations, traits involved in reproduction are more divergent (and more sexually dimorphic) than traits known to be involved in ecological adaptations. Two of the families analyzed in the study by Pfennig and Hurlbert (2012) also demonstrate a correlation between sexual dimorphism and species richness. Finally, in a study more closely focused on one species, Grace and Shaw (2012) show that Vol. 58 Maria R. SERVEDIO Acknowledgments I would like to first and foremost thank the Executive Editor of Current Zoology, Zhiyun Jia, for the enjoyable experience of serving as guest editor on this column, and for all of the invaluable help and advice he has given along the way. I would also like to thank the authors of the articles in the column for their excellent contributions and for being a pleasure to work with. I am grateful to R. Safran for discussion, C. Willett for comments on this manuscript and to NSF DEB-0919018 for funding. References Bolnick DI, Kirkpatrick M, 2012. The relationship between intraspecific assortative mating and reproductive isolation between divergent populations. Curr. Zool. 58 (3): 481–489. Grace JL, Shaw KL, 2012. Incipient sexual isolation in Laupala cerasina: Females discriminate population–level divergence in acoustic characters. Curr. Zool. 58 413–422. Kirkpatrick M, Ravigné V, 2002. Speciation by natural and sexual selection. Am. Nat. 159: S22–S35. Kirkpatrick M, Nuismer SL, 2004. Sexual selection can constrain sympatric speciation. Proc. R. Soc. Lond. B Biol. Sci. 271: 687–693. Kozak GM, Reisland M, Boughman JW, 2009. Sex differences in mate recognition and conspecific preference in species with mutual mate choice. 63: 353–365. Kraaijeveld K, Kraaijeveld-Smit FJ, Maan ME, 2011. Sexual selection and speciation: the comparative evidence revisited. Biol. Rev. 86: 367–377. Lande R, 1981. Models of speciation by sexual selection on polygenic traits. Proc. Natl. Acad. Sci. USA 78: 3721–3725. Maan ME, Seehausen O, 2011. Ecology, sexual selection and speciation 14: 591–602. Macías Garcia C, Smith G, González Zuarth C, Graves JA, Ritchie MG, 2012. Variation in sexual dimorphism and assortative mating do not predict genetic divergence in the sexually dimorphic Goodeid fish Girardinichthys multiradiatus. Curr. Zool. 58 (3): 437–449. Matessi C, Gimelfarb A, Gavrilets S, 2001. Long-term buildup of reproductive isolation promoted by disruptive selection: How far does it go? Selection 2: 41–64. Otto SP, Servedio MR, Nuismer SL, 2008. Frequency-dependent selection and the evolution of assortative mating. Genetics 179: 2091–2112. Panhuis TM, Butlin R, Zuk M, Tregenza T, 2001. Sexual selection and speciation. Trends. Ecol. Evol. 16: 364–371. Pauers MJ, McKinnon JS, 2012. Sexual selection on color and behavior within and between cichlid populations: Implications for speciation. Curr. Zool. 58 (3): 472–480. Pennings PS, Kopp M, Meszena G, Dieckmann U, Hermisson J, 2008. An analytically tractable model for competitive speciation. Am. Nat. 17: E44–E71. Pfennig KS, Hurlbert AH, 2012. Heterospecific interactions and the proliferation of sexually dimorphic traits. Curr. Zool. 58 (3): 450–459. Price T, 1998. Sexual selection and natural selection in bird speciation. Phil. Trans. R. Soc. Lond. B Biol. Sci. 353: 251–260. Qvarnström A, Vallin N, Rudh A. 2012. The role of male contest competition over mates in speciation. Curr. Zool. 58 (3): 490–506. Ritchie MG, 2007. Sexual selection and speciation. Ann. Rev. Ecol. Evol. Syst. 38: 79–102. Rolán Alvarez E, Saura M, Diz AP, Rivas MJ, Alvarez M et al., 2012. Can sexual selection and disassortative mating contribute to the maintenance of a shell color polymorphism in an intertidal marine snail? Curr. Zool. 58 (3): 460–471. Safran R, Flaxman S, Kopp M, Irwin DA, Briggs D, Evans MR, Funk C, Gray DA, Hebets EA, Seddon N, Scordato E, Symes LB, Tobias JA, Toews DPL, Uy JAC, 2012. A robust new metric of phenotypic distance to estimate and compare multiple trait differences among populations. Curr. Zool. 58 (3): 423–436. Servedio MR, Kopp M, 2012. Sexual selection and magic traits in speciation with gene flow. Curr. Zool. 58 (3): 507–513. van Doorn GS, Dieckmann U, Wessing FJ, 2004. Sympatric speciation by sexual selection: A critical reevaluation. Am. Nat. 163: 709–725. Downloaded from https://academic.oup.com/cz/article/58/3/413/1816140 by guest on 13 November 2023 ation with gene flow. While presenting a framework for future analyses, they speculate on whether sexual selection is likely to be a driving force in each of their categories, and come to the overall conclusion that its role may be more limited than previously suggested. The diverse contributions to this column support the suggestion that there is still much work to be done to determine whether sexual selection is very likely to play a causal role in speciation, especially when there is gene flow between incipient species. In many cases the evidence in fact does not support this, which leaves open the interesting idea derived from theoretical studies that sexual selection may sometimes inhibit the speciation process. 415