When does male competition foster speciation?: a comment on Tinghitella et al.

When does male competition foster speciation?: a comment on Tinghitella et al. The review by Tinghitella and colleagues (2018) brings to attention the potentially important role that male competition can have on speciation. Males compete for a limiting resource—the opportunity to mate with females, which can generate very strong divergent selection. A recent study reports divergent selection gradients from male competition substantially stronger than many reported ecological selection gradients (Keagy et al. 2016). However, male competition has not been front and center in work on sexual selection and speciation, despite being a ubiquitous source of strong selection and an arbiter of mating success. This review is timely given several compelling recent papers and mounting evidence. The authors do a nice job covering the importance of geographic context and summarize some key ideas that have been explored, while pointing out fruitful avenues for future work. Here I highlight some additional ideas of when male competition can alter the speciation process. Male competition can have direct effects, but also can modify the effects of mate choice and ecology on speciation. It can either increase or decrease reproductive isolation, or make isolating barriers “leaky” depending on how it interacts with both mate choice and ecological factors. These interactions can be complex. For example, male competition has fostered divergence as reproductive isolation accumulated, but also contributed to the reversal of this process as species fused (Keagy et al. 2016). In another example, the red backed fairy wren mating system is rife with extra pair copulations, and females of both red and orange subspecies choose red males as extra pair mates. Female choice undermines isolation in an asymmetric manner, whereas male competition for territories and mates maintains isolation (Greig et al. 2015). Thus, the two forms of sexual selection combine to allow introgression of red plumage onto the orange genomic background. In this system, male competition enhances isolation, whereas in wall lizards where female choice is weak, male competition causes introgression and depletes reproductive isolation (While et al. 2015). How do we know when male competition helps versus hinders speciation? Not only can we advance by considering both aspects of sexual selection, but also by considering mate choice by both sexes. Males can be choosy, and some theory considers how male competition alters the evolution of male mate choice, which in turn may affect speciation. Typically, male competition limits the evolution of male choice because choosy males compete more for access to preferred females. However, male competition can enhance isolation when choosy males allocate courtship effort strategically in a competitive context, which in turn can create substantial linkage disequilibrium and in some conditions lead to nearly complete assortative mating (Rowell and Servedio 2009). I encourage more theoretical and empirical work considering how male competition affects both female and male choice of mates, and when this enhances or undermines reproductive isolation. Disruptive selection can lead to divergence and reproductive isolation, and the review summarizes some current theory of male competition’s role, which mostly focuses on the effects of frequency-dependent selection. However, frequency-dependent selection has not always been seen when male competition contributes to speciation (Keagy et al. 2016). Moreover, because speciation requires both divergence and reproductive isolation, it is less likely than alternative outcomes such as polymorphism or plasticity (Rueffler et al. 2006). Indeed, intense male competition is a primary cause of alternative mating strategies—polymorphisms in male competitive traits that do not typically cause reproductive isolation. Both theoretical and empirical work to understand when polymorphism versus speciation is likely given ecological and social conditions could bear fruit. One way to make progress may be by emphasizing the relationship between competition for resources (ecological competition) and competition for mates (male competition). The rich body of theoretical and empirical work on ecological competition, niche evolution, and ecological speciation could be leveraged to move our understanding of male competition in speciation forward. Substantial progress has been made adapting ecological principles to study how individual behavioral variation affects reproductive isolation (Bolnick et al. 2003; Boughman and Svanbäck 2017) so this suggestion follows in that tradition. In ecological speciation, resource competition generates disruptive selection generating both premating and ecologically dependent postmating isolation. Although the review restricts itself to premating effects, male competition often continues after mating via sperm or pollen competition also interacting with cryptic female choice, and these dynamic processes can cause substantial prezygotic and postzygotic isolation (Martin and Hosken 2003). There is much intriguing work to be done on the full spectrum of effects male competition can have on the speciation process. REFERENCES Bolnick DI , Svanbäck R , Fordyce JA , Yang LH , Davis JM , Hulsey CD , Forister ML . 2003 . The ecology of individuals: incidence and implications of individual specialization . Am Nat . 161 : 1 – 28 . Google Scholar CrossRef Search ADS PubMed Boughman JW , Svanbäck R . 2017 . Synergistic selection between ecological niche and mate preference primes diversification . Evolution . 71 : 6 – 22 . Google Scholar CrossRef Search ADS PubMed Greig EI , Baldassarre DT , Webster MS . 2015 . Differential rates of phenotypic introgression are associated with male behavioral responses to multiple signals . Evolution . 69 : 2602 – 2612 . Google Scholar CrossRef Search ADS PubMed Keagy J , Lettieri L , Boughman JW . 2016 . Male competition fitness landscapes predict both forward and reverse speciation . Ecol Lett . 19 : 71 – 80 . Google Scholar CrossRef Search ADS PubMed Martin OY , Hosken DJ . 2003 . The evolution of reproductive isolation through sexual conflict . Nature . 423 : 979 – 982 . Google Scholar CrossRef Search ADS PubMed Rowell JT , Servedio MR . 2009 . Gentlemen prefer blondes: the evolution of mate preference among strategically allocated males . Am Nat . 173 : 12 – 25 . Google Scholar CrossRef Search ADS PubMed Rueffler C , Van Dooren TJ , Leimar O , Abrams PA . 2006 . Disruptive selection and then what ? Trends Ecol Evol . 21 : 238 – 245 . Google Scholar CrossRef Search ADS PubMed 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 . 29 : 783 – 797 . Google Scholar CrossRef Search ADS While GM , Michaelides S , Heathcote RJ , MacGregor HE , Zajac N , Beninde J , Carazo P , Pérez I de Lanuza G , Sacchi R , Zuffi MA , et al. 2015 . Sexual selection drives asymmetric introgression in wall lizards . Ecol Lett . 18 : 1366 – 1375 . Google Scholar CrossRef Search ADS PubMed © 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: journals.permissions@oup.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) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Behavioral Ecology Oxford University Press

When does male competition foster speciation?: a comment on Tinghitella et al.

Behavioral Ecology , Volume Advance Article (4) – Apr 4, 2018

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Oxford University Press
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© 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: journals.permissions@oup.com
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1045-2249
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D.O.I.
10.1093/beheco/ary026
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Abstract

The review by Tinghitella and colleagues (2018) brings to attention the potentially important role that male competition can have on speciation. Males compete for a limiting resource—the opportunity to mate with females, which can generate very strong divergent selection. A recent study reports divergent selection gradients from male competition substantially stronger than many reported ecological selection gradients (Keagy et al. 2016). However, male competition has not been front and center in work on sexual selection and speciation, despite being a ubiquitous source of strong selection and an arbiter of mating success. This review is timely given several compelling recent papers and mounting evidence. The authors do a nice job covering the importance of geographic context and summarize some key ideas that have been explored, while pointing out fruitful avenues for future work. Here I highlight some additional ideas of when male competition can alter the speciation process. Male competition can have direct effects, but also can modify the effects of mate choice and ecology on speciation. It can either increase or decrease reproductive isolation, or make isolating barriers “leaky” depending on how it interacts with both mate choice and ecological factors. These interactions can be complex. For example, male competition has fostered divergence as reproductive isolation accumulated, but also contributed to the reversal of this process as species fused (Keagy et al. 2016). In another example, the red backed fairy wren mating system is rife with extra pair copulations, and females of both red and orange subspecies choose red males as extra pair mates. Female choice undermines isolation in an asymmetric manner, whereas male competition for territories and mates maintains isolation (Greig et al. 2015). Thus, the two forms of sexual selection combine to allow introgression of red plumage onto the orange genomic background. In this system, male competition enhances isolation, whereas in wall lizards where female choice is weak, male competition causes introgression and depletes reproductive isolation (While et al. 2015). How do we know when male competition helps versus hinders speciation? Not only can we advance by considering both aspects of sexual selection, but also by considering mate choice by both sexes. Males can be choosy, and some theory considers how male competition alters the evolution of male mate choice, which in turn may affect speciation. Typically, male competition limits the evolution of male choice because choosy males compete more for access to preferred females. However, male competition can enhance isolation when choosy males allocate courtship effort strategically in a competitive context, which in turn can create substantial linkage disequilibrium and in some conditions lead to nearly complete assortative mating (Rowell and Servedio 2009). I encourage more theoretical and empirical work considering how male competition affects both female and male choice of mates, and when this enhances or undermines reproductive isolation. Disruptive selection can lead to divergence and reproductive isolation, and the review summarizes some current theory of male competition’s role, which mostly focuses on the effects of frequency-dependent selection. However, frequency-dependent selection has not always been seen when male competition contributes to speciation (Keagy et al. 2016). Moreover, because speciation requires both divergence and reproductive isolation, it is less likely than alternative outcomes such as polymorphism or plasticity (Rueffler et al. 2006). Indeed, intense male competition is a primary cause of alternative mating strategies—polymorphisms in male competitive traits that do not typically cause reproductive isolation. Both theoretical and empirical work to understand when polymorphism versus speciation is likely given ecological and social conditions could bear fruit. One way to make progress may be by emphasizing the relationship between competition for resources (ecological competition) and competition for mates (male competition). The rich body of theoretical and empirical work on ecological competition, niche evolution, and ecological speciation could be leveraged to move our understanding of male competition in speciation forward. Substantial progress has been made adapting ecological principles to study how individual behavioral variation affects reproductive isolation (Bolnick et al. 2003; Boughman and Svanbäck 2017) so this suggestion follows in that tradition. In ecological speciation, resource competition generates disruptive selection generating both premating and ecologically dependent postmating isolation. Although the review restricts itself to premating effects, male competition often continues after mating via sperm or pollen competition also interacting with cryptic female choice, and these dynamic processes can cause substantial prezygotic and postzygotic isolation (Martin and Hosken 2003). There is much intriguing work to be done on the full spectrum of effects male competition can have on the speciation process. REFERENCES Bolnick DI , Svanbäck R , Fordyce JA , Yang LH , Davis JM , Hulsey CD , Forister ML . 2003 . The ecology of individuals: incidence and implications of individual specialization . Am Nat . 161 : 1 – 28 . Google Scholar CrossRef Search ADS PubMed Boughman JW , Svanbäck R . 2017 . Synergistic selection between ecological niche and mate preference primes diversification . Evolution . 71 : 6 – 22 . Google Scholar CrossRef Search ADS PubMed Greig EI , Baldassarre DT , Webster MS . 2015 . Differential rates of phenotypic introgression are associated with male behavioral responses to multiple signals . Evolution . 69 : 2602 – 2612 . Google Scholar CrossRef Search ADS PubMed Keagy J , Lettieri L , Boughman JW . 2016 . Male competition fitness landscapes predict both forward and reverse speciation . Ecol Lett . 19 : 71 – 80 . Google Scholar CrossRef Search ADS PubMed Martin OY , Hosken DJ . 2003 . The evolution of reproductive isolation through sexual conflict . Nature . 423 : 979 – 982 . Google Scholar CrossRef Search ADS PubMed Rowell JT , Servedio MR . 2009 . Gentlemen prefer blondes: the evolution of mate preference among strategically allocated males . Am Nat . 173 : 12 – 25 . Google Scholar CrossRef Search ADS PubMed Rueffler C , Van Dooren TJ , Leimar O , Abrams PA . 2006 . Disruptive selection and then what ? Trends Ecol Evol . 21 : 238 – 245 . Google Scholar CrossRef Search ADS PubMed 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 . 29 : 783 – 797 . Google Scholar CrossRef Search ADS While GM , Michaelides S , Heathcote RJ , MacGregor HE , Zajac N , Beninde J , Carazo P , Pérez I de Lanuza G , Sacchi R , Zuffi MA , et al. 2015 . Sexual selection drives asymmetric introgression in wall lizards . Ecol Lett . 18 : 1366 – 1375 . Google Scholar CrossRef Search ADS PubMed © 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: journals.permissions@oup.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)

Journal

Behavioral EcologyOxford University Press

Published: Apr 4, 2018

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