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McCullough and Emlen • The research bias is unfortunate but also unsurprising 801 Let us assume that females mate indiscriminately, accepting as Divergence is not speciation, or why mates males successful in male–male competition, in whatever we need females: a comment on form. In this case, it is not immediately clear why the nature (or Tinghitella et al. extent) of that male–male competition should influence reproduc - tive isolation. Even if populations diverge in male–male competi- a,b c, Emily R. Burdfield-Steel and David M. Shuker tion traits, on secondary contact indiscriminate females from either Centre of Excellence in Biological Interactions, Department of population should mate with successful males, breaking down pop- Biological and Environmental Science, P.O. Box 35, 40014 University ulation barriers. On the other hand, if females have preferences of Jyväskylä, Finland, Department of Biological Sciences, Faculty for male traits also involved in male–male competition, then these of Science, Macquarie University, North Ryde NSW 2008, Australia, preferences may well limit the scope for divergence in those traits. and School of Biology, University of St Andrews, Harold Mitchell While Tinghitella et al. (2018) mention how male–male competi- Building, St Andrews, KY16 9TH, UK tion will likely interact with mate choice (and natural selection) if it is to influence RI, we suggest that considering the role of male– Tinghitella et al. (2018) provide a wonderful review of the role of male competition in prezygotic isolation will only be relevant in male–male competition in the divergence of traits across popula- terms of the context of male–female interactions, because of the tions. Using a range of examples, the authors show how male traits need to bias which females mate with which males for RI to occur. associated with intrasexual competition for mates can diverge. In summary, in terms of postzygotic incompatibilities, male– They also show that, in a few examples, male–male competition male competition may, like all aspects of selection, generate genetic can interact with other processes—such as mate choice or natural incompatibilities among diverging populations yielding RI. In this selection on ecologically relevant traits—to influence how repro - context, male–male competition should neither be ignored nor be ductive isolation (RI) may come about. In this comment, we wish to considered a particularly special part of speciation. In terms of build on that latter aspect, and emphasize that divergence itself is prezygotic incompatibilities, sex and gene flow means that females not enough for speciation. We note from the outset that the authors will nearly always play an integral role in influencing how male– caution this, but we wish to add further emphasis, as it has impor- male competition influences reproductive isolation, and so females tant ramifications for the role of males and females in speciation. will typically have the last word on how males influence speciation. Divergence is not speciation. Something else is needed to close the loop, so that diverging populations become separate species. Address correspondence to D.M. Shuker. E-mail: david.shuker@st-andrews. Under common definitions of species, that something else is one or ac.uk. more forms of RI (Coyne and Orr 2004). In other words, among- population variation in phenotypes and genotypes is not speciation Received 29 December 2017; revised 17 April 2018; editorial decision 17 April 2018; accepted 30 April 2018; Advance Access publication 9 May 2018 until something about those phenotypes or genotypes limits gene flow absolutely, or at least to negligible levels. Typically, we envisage doi:10.1093/beheco/ary069 pre- or postzygotic RI, with prezygotic isolation occurring as either Editor-in-Chief: Leigh Simmons precopulatory or postcopulatory mechanisms of isolation. The question therefore is not whether male–male competition traits diverge (they do), but rather how they influence RI. REFERENCES As briefly mentioned by Tinghitella et al. (2018), the simplest Coyne JA, Orr HA. 2004 Speciation. Sunderland (MA): Sinauer. situation is when changes in male–male competitive phenotypes Heathcote RJ, While GM, MacGregor HE, Sciberras J, Leroy C, D’Ettorre involve genetic changes that lead to postzygotic genetic incompat- P, Uller T. 2016. Male behaviour drives assortative reproduction during the initial stage of secondary contact. J Evol Biol. 29:1003–1015. ibilities, such that individuals from divergent populations mate and Martin MD, Mendelson TC. 2016. Male behaviour predicts trait diver- produce unfit or inviable hybrids. This loss of fitness may be due gence and the evolution of reproductive isolation in darters (Percidae: to the production of sons that are unable to compete effectively (a Etheostoma). Anim Behav. 112:179–186. form of extrinsic incompatibility). Alternatively, the loss of fitness Parker GA, Partridge L. 1998. Sexual conflict and speciation. Philos Trans R Soc Lond B Biol Sci. 353:261–274. may involve mutations not obviously associated phenotypically Simmons LW. 2018. Sperm competition, sexual conflict, and speciation: a with male–male competition, in the extreme case being lethal in comment on Tinghitella et al. Behav Ecol. 29:800. hybrid genetic backgrounds (a form of intrinsic incompatibility). Tinghitella RM, Lackey ACR, Martin M, Dijkstra PD, Drury JP, Heathcote Of course, any evolutionary change can lead to such incompat- R, Keagy J, Scordato ESC, Tyers AM. 2018. On the role of male ibilities, and so in this sense male–male competition joins all forms competition in speciation: a review and research agenda. Behav Ecol. 29:783–797. of selection as a source of RI and therefore a “process” of spe- ciation. However, we feel that the emphasis of Tinghitella et al. (2018) is more specific, focusing on sexual selection and prezygotic isolation. With prezygotic isolation, we need the divergence in male traits When does male competition foster to either lead to isolation independently of females, or via female– speciation?: a comment on Tinghitella et al. male interactions. Our discussion will be quite general, although we note that perhaps the most likely venue for such effects is in Janette W. Boughman the postcopulatory sphere (see Simmons 2018). Tinghitella et al. Department of Integrative Biology, Natural Sciences 203, 288 Farm (2018) discuss how male–male competition might lead to reproduc- Lane, Michigan State University, East Lansing, MI 48824, USA tive isolation without females, although perhaps their most convinc- ing examples also include male mate choice (Heathcote et al. 2016; The review by Tinghitella and colleagues (2018) brings to attention Martin and Mendelson 2016). But let’s take a step back and con- the potentially important role that male competition can have on sider the situation more from a mating systems perspective than a speciation. Males compete for a limiting resource—the opportu- speciation one (see also Parker and Partridge 1998). nity to mate with females, which can generate very strong divergent Downloaded from https://academic.oup.com/beheco/article-abstract/29/4/801/4994267 by Ed 'DeepDyve' Gillespie user on 11 July 2018
Behavioral Ecology – Oxford University Press
Published: May 9, 2018
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