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A major player need not be the only player in speciation: a response to comments on Tinghitella et al.

A major player need not be the only player in speciation: a response to comments on Tinghitella... We are delighted that our recent review (Tinghitella et al. 2018) has garnered broad interest and thoughtful commentary. Collectively, it is clear that the link between competition for mates and divergence in competitive phenotypes is well supported. As we and the invited commentary authors point out, it is less clear when mate competition can and is most likely to cause reproductive isolation. Here, we wish to highlight some solutions offered by the Invited Commentaries, and to reiterate that while competition for mates might not act alone to cause speciation, ignoring it altogether will leave gaps in our understanding because mate competition may initiate, enhance, stabilize, or hinder divergence. After all, ecological speciation requires assortative mating, and sexual selection via mate choice is less likely to cause speciation in the absence of ecological divergence. What is the range of scenarios under which competition for mates can contribute to reproductive isolation? As McCullough and Emlen (2018) point out, the unclear relationship between male competition and reproductive isolation is largely responsible for the absence of male competition in the speciation literature. Simmons (2018) helps to fill this gap by considering postcopulatory sperm competition and the potential for sexual conflict. These coupled processes can result in divergence between lineages in genital morphology and male–female postcopulatory molecular interactions, generating rapid evolution of reproductive isolation. It is more difficult to determine how precopulatory male competition could result in reproductive isolation. The best studied mechanism is negative frequency-dependent selection of competitive phenotypes, which can generate distinct morphs and favor assortative mating via selection against hybrids and reinforcement (Dijkstra and Border 2018). Burdfield-Steel and Shuker (2018) emphasize the centrality of reproductive isolation to speciation and offer that females must be the ultimate arbiters of isolation. We agree that speciation by male competition would be most likely under circumstances that link mate choice to competitive traits. But, females need not be the choosy sex. Recent work suggests a dual role for males in speciation as both competitors and choosers (Boughman 2018; Tinghitella et al. 2018). Male darter fish, for instance, compete for access to females and display divergent male color patterns that have coevolved with competitive responses. Yet, male darters are also the choosier sex in an interspecific context (Mendelson et al. 2018). So, though male–female interactions are likely integral to speciation by male competition, it may be more accurate to assume the need for competitors and choosers, whether or not these roles are filled by 1 or 2 sexes. Lehtonen (2018) and Simmons (2018) call for embedding our understanding of the role of competition for mates in the context of different mating systems because the strength and nature of selection on competitors’ traits should depend on the opportunity to monopolize mates. In polygynous or polyandrous mating systems, the potential to monopolize mates is high and, thus, intrasexual competition significantly affects mating success. Strong male competition is most likely in polygynous systems, and pre and postcopulatory sexual selection resulting from this competition should be greater in systems with more male-biased operational sex ratios. Although polyandry is expected to decrease the strength of male competition (Simmons 2018), it should increase the strength of female competition, which can also contribute to divergence and speciation (Lipshutz 2018). Importantly, in systems where males and females have multiple mates, both male and female intrasexual selection can occur. Intrasexual competition in both sexes could facilitate speciation via frequency-dependent intrasexual selection and mate choice (van Doorn et al. 2004) or via sexual conflict (Simmons 2018). Lehtonen (2018) pushes further, blurring the lines between ecological and sexual competition (Boughman 2018; Dijkstra and Border 2018), to discuss how competition among socially monogamous mated pairs (instead of individuals) for resources could lead to speciation. In summary, we advocate a holistic approach to speciation research that carefully considers the biology of the study system and the processes likely to be at play. Such an approach should include broad thinking about interacting mechanisms and sex-specific mating strategies, and thoughtful consideration of both pre and postcopulatory mate competition. Speciation is perhaps the greatest show on Earth, but we have not been paying attention to all the players driving this performance. When we do, our appreciation and understanding will be that much more complete. REFERENCES Boughman JW . 2018 . When does male competition foster speciation? A comment on Tinghitella et al . Behav Ecol . 29 : 801 – 802 . Google Scholar CrossRef Search ADS Burdfield-Steel ER , Shuker DM . 2018 . Divergence is not speciation, or why we need females: a comments on Tinghitella et al . Behav Ecol . 29 : 801 . Google Scholar CrossRef Search ADS Dijkstra PD , Border SE . 2018 . How does male-male competition generate negative frequency-dependent selection and disruptive selection during speciation ? Curr Zool . 64 : 89 – 99 . Google Scholar CrossRef Search ADS PubMed van Doorn SG , Dieckmann U , Weissing FJ . 2004 . Sympatric speciation by sexual selection: a critical reevaluation . Am Nat . 163 : 709 – 725 . Google Scholar CrossRef Search ADS PubMed Lehtonen TK . 2018 . What is the role of competition among pairs in speciation?: a comments on Tinghitella et al . Behav Ecol . 29 : 799 . Google Scholar CrossRef Search ADS Lipshutz SE . 2018 . Interspecific competition, hybridization, and reproductive isolation in secondary contact: missing perspectives on males and females . Curr Zool . 64 : 75 – 88 . Google Scholar CrossRef Search ADS PubMed McCullough EL , Emlen DJ . 2018 . The research bias is unfortunate but also unsurprising: a comment on Tinghitella et al . Behav Ecol . 29 : 798 . Google Scholar CrossRef Search ADS Mendelson TC , Gumm JM , Martin MD , Ciccotto PJ . 2018 . Preference for conspecifics evolves earlier in males than females in a sexually dimorphic radiation of fishes . Evolution . 72 : 337 – 347 . Google Scholar CrossRef Search ADS PubMed Simmons LW . 2018 . Sperm competition, sexual conflict, and speciation: a comment on Tinghitella et al . Behav Ecol . 29 : 800 . Google Scholar CrossRef Search ADS Tinghitella RM , Lackey ACR , Martin M , Dijkstra PD , Drury JP , Heathcote R , Scordato ESC , Tyers AM . 2018 . On the role of male competition in speciation: a review and research agenda . Behav Ecol . 29 : 783 – 797 . Google Scholar CrossRef Search ADS © 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 protected] 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) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Behavioral Ecology Oxford University Press

A major player need not be the only player in speciation: a response to comments on Tinghitella et al.

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Publisher
Oxford University Press
Copyright
© 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 protected]
ISSN
1045-2249
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1465-7279
DOI
10.1093/beheco/ary051
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Abstract

We are delighted that our recent review (Tinghitella et al. 2018) has garnered broad interest and thoughtful commentary. Collectively, it is clear that the link between competition for mates and divergence in competitive phenotypes is well supported. As we and the invited commentary authors point out, it is less clear when mate competition can and is most likely to cause reproductive isolation. Here, we wish to highlight some solutions offered by the Invited Commentaries, and to reiterate that while competition for mates might not act alone to cause speciation, ignoring it altogether will leave gaps in our understanding because mate competition may initiate, enhance, stabilize, or hinder divergence. After all, ecological speciation requires assortative mating, and sexual selection via mate choice is less likely to cause speciation in the absence of ecological divergence. What is the range of scenarios under which competition for mates can contribute to reproductive isolation? As McCullough and Emlen (2018) point out, the unclear relationship between male competition and reproductive isolation is largely responsible for the absence of male competition in the speciation literature. Simmons (2018) helps to fill this gap by considering postcopulatory sperm competition and the potential for sexual conflict. These coupled processes can result in divergence between lineages in genital morphology and male–female postcopulatory molecular interactions, generating rapid evolution of reproductive isolation. It is more difficult to determine how precopulatory male competition could result in reproductive isolation. The best studied mechanism is negative frequency-dependent selection of competitive phenotypes, which can generate distinct morphs and favor assortative mating via selection against hybrids and reinforcement (Dijkstra and Border 2018). Burdfield-Steel and Shuker (2018) emphasize the centrality of reproductive isolation to speciation and offer that females must be the ultimate arbiters of isolation. We agree that speciation by male competition would be most likely under circumstances that link mate choice to competitive traits. But, females need not be the choosy sex. Recent work suggests a dual role for males in speciation as both competitors and choosers (Boughman 2018; Tinghitella et al. 2018). Male darter fish, for instance, compete for access to females and display divergent male color patterns that have coevolved with competitive responses. Yet, male darters are also the choosier sex in an interspecific context (Mendelson et al. 2018). So, though male–female interactions are likely integral to speciation by male competition, it may be more accurate to assume the need for competitors and choosers, whether or not these roles are filled by 1 or 2 sexes. Lehtonen (2018) and Simmons (2018) call for embedding our understanding of the role of competition for mates in the context of different mating systems because the strength and nature of selection on competitors’ traits should depend on the opportunity to monopolize mates. In polygynous or polyandrous mating systems, the potential to monopolize mates is high and, thus, intrasexual competition significantly affects mating success. Strong male competition is most likely in polygynous systems, and pre and postcopulatory sexual selection resulting from this competition should be greater in systems with more male-biased operational sex ratios. Although polyandry is expected to decrease the strength of male competition (Simmons 2018), it should increase the strength of female competition, which can also contribute to divergence and speciation (Lipshutz 2018). Importantly, in systems where males and females have multiple mates, both male and female intrasexual selection can occur. Intrasexual competition in both sexes could facilitate speciation via frequency-dependent intrasexual selection and mate choice (van Doorn et al. 2004) or via sexual conflict (Simmons 2018). Lehtonen (2018) pushes further, blurring the lines between ecological and sexual competition (Boughman 2018; Dijkstra and Border 2018), to discuss how competition among socially monogamous mated pairs (instead of individuals) for resources could lead to speciation. In summary, we advocate a holistic approach to speciation research that carefully considers the biology of the study system and the processes likely to be at play. Such an approach should include broad thinking about interacting mechanisms and sex-specific mating strategies, and thoughtful consideration of both pre and postcopulatory mate competition. Speciation is perhaps the greatest show on Earth, but we have not been paying attention to all the players driving this performance. When we do, our appreciation and understanding will be that much more complete. REFERENCES Boughman JW . 2018 . When does male competition foster speciation? A comment on Tinghitella et al . Behav Ecol . 29 : 801 – 802 . Google Scholar CrossRef Search ADS Burdfield-Steel ER , Shuker DM . 2018 . Divergence is not speciation, or why we need females: a comments on Tinghitella et al . Behav Ecol . 29 : 801 . Google Scholar CrossRef Search ADS Dijkstra PD , Border SE . 2018 . How does male-male competition generate negative frequency-dependent selection and disruptive selection during speciation ? Curr Zool . 64 : 89 – 99 . Google Scholar CrossRef Search ADS PubMed van Doorn SG , Dieckmann U , Weissing FJ . 2004 . Sympatric speciation by sexual selection: a critical reevaluation . Am Nat . 163 : 709 – 725 . Google Scholar CrossRef Search ADS PubMed Lehtonen TK . 2018 . What is the role of competition among pairs in speciation?: a comments on Tinghitella et al . Behav Ecol . 29 : 799 . Google Scholar CrossRef Search ADS Lipshutz SE . 2018 . Interspecific competition, hybridization, and reproductive isolation in secondary contact: missing perspectives on males and females . Curr Zool . 64 : 75 – 88 . Google Scholar CrossRef Search ADS PubMed McCullough EL , Emlen DJ . 2018 . The research bias is unfortunate but also unsurprising: a comment on Tinghitella et al . Behav Ecol . 29 : 798 . Google Scholar CrossRef Search ADS Mendelson TC , Gumm JM , Martin MD , Ciccotto PJ . 2018 . Preference for conspecifics evolves earlier in males than females in a sexually dimorphic radiation of fishes . Evolution . 72 : 337 – 347 . Google Scholar CrossRef Search ADS PubMed Simmons LW . 2018 . Sperm competition, sexual conflict, and speciation: a comment on Tinghitella et al . Behav Ecol . 29 : 800 . Google Scholar CrossRef Search ADS Tinghitella RM , Lackey ACR , Martin M , Dijkstra PD , Drury JP , Heathcote R , Scordato ESC , Tyers AM . 2018 . On the role of male competition in speciation: a review and research agenda . Behav Ecol . 29 : 783 – 797 . Google Scholar CrossRef Search ADS © 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 protected] 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)

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Behavioral Ecology – Oxford University Press

Published: Apr 6, 2018

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