Tinghitella et al. (2018) provide a wonderful review of the role of male–male competition in the divergence of traits across populations. Using a range of examples, the authors show how male traits associated with intrasexual competition for mates can diverge. They also show that, in a few examples, male–male competition can interact with other processes—such as mate choice or natural selection on ecologically relevant traits—to influence how reproductive isolation (RI) may come about. In this comment, we wish to build on that latter aspect, and emphasize that divergence itself is not enough for speciation. We note from the outset that the authors caution this, but we wish to add further emphasis, as it has important ramifications for the role of males and females in speciation. Divergence is not speciation. Something else is needed to close the loop, so that diverging populations become separate species. Under common definitions of species, that something else is one or more forms of RI (Coyne and Orr 2004). In other words, among-population variation in phenotypes and genotypes is not speciation until something about those phenotypes or genotypes limits gene flow absolutely, or at least to negligible levels. Typically, we envisage pre- or postzygotic RI, with prezygotic isolation occurring as either 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. As briefly mentioned by Tinghitella et al. (2018), the simplest situation is when changes in male–male competitive phenotypes involve genetic changes that lead to postzygotic genetic incompatibilities, such that individuals from divergent populations mate and produce unfit or inviable hybrids. This loss of fitness may be due to the production of sons that are unable to compete effectively (a form of extrinsic incompatibility). Alternatively, the loss of fitness may involve mutations not obviously associated phenotypically with male–male competition, in the extreme case being lethal in hybrid genetic backgrounds (a form of intrinsic incompatibility). Of course, any evolutionary change can lead to such incompatibilities, and so in this sense male–male competition joins all forms of selection as a source of RI and therefore a “process” of speciation. 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 to either lead to isolation independently of females, or via female–male interactions. Our discussion will be quite general, although we note that perhaps the most likely venue for such effects is in the postcopulatory sphere (see Simmons 2018). Tinghitella et al. (2018) discuss how male–male competition might lead to reproductive isolation without females, although perhaps their most convincing examples also include male mate choice (Heathcote et al. 2016; Martin and Mendelson 2016). But let’s take a step back and consider the situation more from a mating systems perspective than a speciation one (see also Parker and Partridge 1998). Let us assume that females mate indiscriminately, accepting as mates males successful in male–male competition, in whatever form. In this case, it is not immediately clear why the nature (or extent) of that male–male competition should influence reproductive isolation. Even if populations diverge in male–male competition traits, on secondary contact indiscriminate females from either population should mate with successful males, breaking down population barriers. On the other hand, if females have preferences for male traits also involved in male–male competition, then these preferences may well limit the scope for divergence in those traits. While Tinghitella et al. (2018) mention how male–male competition will likely interact with mate choice (and natural selection) if it is to influence RI, we suggest that considering the role of male–male competition in prezygotic isolation will only be relevant in terms of the context of male–female interactions, because of the need to bias which females mate with which males for RI to occur. In summary, in terms of postzygotic incompatibilities, male–male competition may, like all aspects of selection, generate genetic incompatibilities among diverging populations yielding RI. In this context, male–male competition should neither be ignored nor be considered a particularly special part of speciation. In terms of prezygotic incompatibilities, sex and gene flow means that females will nearly always play an integral role in influencing how male–male competition influences reproductive isolation, and so females will typically have the last word on how males influence speciation. References Coyne JA, Orr HA. 2004 Speciation . Sunderland (MA): Sinauer. Heathcote RJ, While GM, MacGregor HE, Sciberras J, Leroy C, D’Ettorre P, Uller T. 2016. Male behaviour drives assortative reproduction during the initial stage of secondary contact. J Evol Biol . 29: 1003– 1015. Google Scholar CrossRef Search ADS PubMed Martin MD, Mendelson TC. 2016. Male behaviour predicts trait divergence and the evolution of reproductive isolation in darters (Percidae: Etheostoma). Anim Behav . 112: 179– 186. Google Scholar CrossRef Search ADS Parker GA, Partridge L. 1998. Sexual conflict and speciation. Philos Trans R Soc Lond B Biol Sci . 353: 261– 274. Google Scholar CrossRef Search ADS PubMed Simmons LW. 2018. Sperm competition, sexual conflict, and speciation: a comment on Tinghitella et al. Behav Ecol . doi: 10.1093/beheco/arx171. Tinghitella RM, Lackey ACR, Martin M, Dijkstra PD, Drury JP, Heathcote R, Keagy J, Scordato ESC, Tyers AM. 2018. On the role of male competition in speciation: a review and research agenda. Behav Ecol . doi: 10.1093/beheco/arx151. © The Author(s) 2018. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: email@example.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)
Behavioral Ecology – Oxford University Press
Published: May 9, 2018
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