Sperm competition, sexual conflict, and speciation: a comment on Tinghitella et al.

Sperm competition, sexual conflict, and speciation: a comment on Tinghitella et al. 800 Behavioral Ecology frequency below that which is optimal for lifetime reproductive Sperm competition, sexual conflict, success. Seminal fluid proteins that promote male fitness can even and speciation: a comment on be toxic, reducing female lifespan. Sexual selection via sperm Tinghitella et al. competition is also known to favor increased numbers of sperm in the ejaculate, and sperm that have increased fertilization capac- Leigh W. Simmons ity (Simmons 2001). High densities of competitive sperm can Centre for Evolutionary Biology, School of Biological Sciences be detrimental to female fitness when they result in polyspermy (M092), (Arnqvist and Rowe 2005). The University of Western Australia, 35 Stirling Highway, Crawley Whenever male sperm competition traits have negative fitness 6008, Australia consequences for females, selection will favor counter adaptations in females to resist male harm. Counter adaptations might include While Darwin’s theory of sexual selection via male contest compe- changes in the shape or thickness of the female reproductive tract, tition was readily accepted as an evolutionary driving force, female reproductive tract proteins that denature the seminal fluid pro - choice was not. The initial rejection of female choice initiated over teins delivered by males, or increased resistance to fertilization by 100  years of theoretical and empirical research effort that has cul - ova (Arnqvist and Rowe 2005). Postmating sexual selection acting minated in a rich appreciation of female choice as an engine of spe- on males can thereby generate cycles of antagonistic coevolution ciation. But as (Tinghitella et  al. 2018) rightly highlight, the intense between males and females that can drive extremely rapid evolu- focus on female choice has been accompanied by a neglect of the tionary divergence and speciation, both in sympatry (Gavrilets and role of male contest competition in the speciation process. Tinghitella Waxman 2002) and allopatry (Gavrilets 2000). Indeed, comparative et al. (2018) provide a timely overview of the various mechanisms by analyses have revealed greater species diversity among clades of which sexual selection through male contest competition might gen- insect with postmating sexual selection compared with clades where erate phenotypic divergence among and within populations, and pro- females mate only once (Arnqvist et al. 2000). vide us with a research agenda with which to redress the balance in Arnqvist and Rowe (2005) suggest that postmating sexually research effort on the evolutionary consequences of Darwin’s other antagonistic coevolution may be a more potent driver of specia- mechanism of sexual selection. What Darwin did not appreciate was tion than other forms of intersexual selection because selection on that sexual selection continues beyond mate acquisition, in the form females will be direct, via the costs of sperm competition traits in of sperm competition and cryptic female choice (Simmons 2001). males, rather than indirect through the benefits required by models While Tinghitella et  al.’s review focused on male competition prior of female choice. Sperm competition may also be a more powerful to mating, it is important to highlight the evolutionary consequences driver of speciation than male contest competition. When females of sperm competition for speciation, and its interplay with premating mate multiply, the strength of premating sexual selection acting on male contest competition. males will be greatly diluted (Parker and Birkhead 2013). A  gen- When females mate with more than one male, sexual selection will eral understanding of the role of male competition in speciation favor adaptations in males that allow them to pre-empt the sperm must therefore encompass mechanisms of sexual selection operat- stored by females from rival males and prevent females from accept- ing before, during, and after mating. ing further matings that might result in the loss of paternity (Simmons 2001). For example, male intromittent genitalia can function in the removal of rival sperm during copulation such that males with genital Address correspondence to L.W. Simmons. E-mail: leigh.simmons@uwa.edu.au. morphology better equipped to remove rival sperm gain a selective Received 13 November 2017; accepted 17 November 2017.; editorial advantage during fertilization. As noted by Tinghitella et  al. (2018) decision 16 November 2017; Advance Access publication 19 December 2017 populations can vary in operational sex ratio or density, both factors doi:10.1093/beheco/arx171 which are known to affect the risk and intensity of sperm competi - tion and selection for male expenditure on sperm competition traits Editor-in-Chief: Leigh Simmons (Simmons 2001). Population divergence in male genital traits used in sperm competition with rivals can result in mechanical incompatibili- ties among populations when they come together, imposing reproduc- tive isolation and speciation (e.g., Wojcieszek and Simmons 2013). REFERENCES Male adaptations for sperm competition may not always be in Arnqvist G, Edvardsson M, Friberg U, Nilsson T. 2000. Sexual con- the best interests of females. Male seminal fluid proteins can pro - flict promotes speciation in insects. Proc Natl Acad Sci USA. 97: foundly affect female reproductive physiology, promoting rapid 10460–10464. Arnqvist G, Rowe L. 2005. Sexual conflict. New Jersey: Princeton egg deposition and/or inhibiting female sexual receptivity to University Press. rival males (Arnqvist and Rowe 2005). In this way, seminal fluid Gavrilets S. 2000. Rapid evolution of reproductive barriers driven by sexual proteins represent an important weapon in the arsenal of male conflict. Nature. 403:886–889. postmating competition for fertilizations. In some species, semi- Gavrilets S, Waxman D. 2002. Sympatric speciation by sexual conflict. Proc Natl Acad Sci USA. 99:10533–10538. nal fluid proteins are absorbed through the female’s reproduc - Parker GA, Birkhead TR. 2013. Polyandry: the history of a revolution. tive tract and into her blood stream, while in others, the male’s Philos Trans R Soc Lond B Biol Sci. 368:20120335. genitalia can pierce the female’s reproductive tract allowing direct Simmons LW, 2001. Sperm competition and its evolutionary consequences access of seminal fluid to her body cavity. Importantly, seminal in the insects. Princeton: Princeton University Press. fluids that benefit males in postmating sperm competition are Tinghitella RM, Lackey ACR, Martin M, Dijkstra PD, Drury JP, Heathcote R, Keagy J, Scordato ESC, Tyers AM, 2018. On the role of male competi- frequently costly for females (Arnqvist and Rowe 2005). Females tion in speciation: a review and research agenda. Behav Ecol. 29:783–797. can suffer energetic costs associated with reproductive tract Wojcieszek JM, Simmons LW. 2013. Divergence in genital morphology may wound repair, they can be exposed to pathogens during traumatic contribute to mechanical reproductive isolation in a millipede. Ecol Evol. insemination, or seminal fluid proteins can reduce female mating 3:334–343. Downloaded from https://academic.oup.com/beheco/article-abstract/29/4/800/4762157 by Ed 'DeepDyve' Gillespie user on 11 July 2018 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Behavioral Ecology Oxford University Press

Sperm competition, sexual conflict, and speciation: a comment on Tinghitella et al.

Behavioral Ecology , Volume Advance Article (4) – Dec 19, 2017
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Abstract

800 Behavioral Ecology frequency below that which is optimal for lifetime reproductive Sperm competition, sexual conflict, success. Seminal fluid proteins that promote male fitness can even and speciation: a comment on be toxic, reducing female lifespan. Sexual selection via sperm Tinghitella et al. competition is also known to favor increased numbers of sperm in the ejaculate, and sperm that have increased fertilization capac- Leigh W. Simmons ity (Simmons 2001). High densities of competitive sperm can Centre for Evolutionary Biology, School of Biological Sciences be detrimental to female fitness when they result in polyspermy (M092), (Arnqvist and Rowe 2005). The University of Western Australia, 35 Stirling Highway, Crawley Whenever male sperm competition traits have negative fitness 6008, Australia consequences for females, selection will favor counter adaptations in females to resist male harm. Counter adaptations might include While Darwin’s theory of sexual selection via male contest compe- changes in the shape or thickness of the female reproductive tract, tition was readily accepted as an evolutionary driving force, female reproductive tract proteins that denature the seminal fluid pro - choice was not. The initial rejection of female choice initiated over teins delivered by males, or increased resistance to fertilization by 100  years of theoretical and empirical research effort that has cul - ova (Arnqvist and Rowe 2005). Postmating sexual selection acting minated in a rich appreciation of female choice as an engine of spe- on males can thereby generate cycles of antagonistic coevolution ciation. But as (Tinghitella et  al. 2018) rightly highlight, the intense between males and females that can drive extremely rapid evolu- focus on female choice has been accompanied by a neglect of the tionary divergence and speciation, both in sympatry (Gavrilets and role of male contest competition in the speciation process. Tinghitella Waxman 2002) and allopatry (Gavrilets 2000). Indeed, comparative et al. (2018) provide a timely overview of the various mechanisms by analyses have revealed greater species diversity among clades of which sexual selection through male contest competition might gen- insect with postmating sexual selection compared with clades where erate phenotypic divergence among and within populations, and pro- females mate only once (Arnqvist et al. 2000). vide us with a research agenda with which to redress the balance in Arnqvist and Rowe (2005) suggest that postmating sexually research effort on the evolutionary consequences of Darwin’s other antagonistic coevolution may be a more potent driver of specia- mechanism of sexual selection. What Darwin did not appreciate was tion than other forms of intersexual selection because selection on that sexual selection continues beyond mate acquisition, in the form females will be direct, via the costs of sperm competition traits in of sperm competition and cryptic female choice (Simmons 2001). males, rather than indirect through the benefits required by models While Tinghitella et  al.’s review focused on male competition prior of female choice. Sperm competition may also be a more powerful to mating, it is important to highlight the evolutionary consequences driver of speciation than male contest competition. When females of sperm competition for speciation, and its interplay with premating mate multiply, the strength of premating sexual selection acting on male contest competition. males will be greatly diluted (Parker and Birkhead 2013). A  gen- When females mate with more than one male, sexual selection will eral understanding of the role of male competition in speciation favor adaptations in males that allow them to pre-empt the sperm must therefore encompass mechanisms of sexual selection operat- stored by females from rival males and prevent females from accept- ing before, during, and after mating. ing further matings that might result in the loss of paternity (Simmons 2001). For example, male intromittent genitalia can function in the removal of rival sperm during copulation such that males with genital Address correspondence to L.W. Simmons. E-mail: leigh.simmons@uwa.edu.au. morphology better equipped to remove rival sperm gain a selective Received 13 November 2017; accepted 17 November 2017.; editorial advantage during fertilization. As noted by Tinghitella et  al. (2018) decision 16 November 2017; Advance Access publication 19 December 2017 populations can vary in operational sex ratio or density, both factors doi:10.1093/beheco/arx171 which are known to affect the risk and intensity of sperm competi - tion and selection for male expenditure on sperm competition traits Editor-in-Chief: Leigh Simmons (Simmons 2001). Population divergence in male genital traits used in sperm competition with rivals can result in mechanical incompatibili- ties among populations when they come together, imposing reproduc- tive isolation and speciation (e.g., Wojcieszek and Simmons 2013). REFERENCES Male adaptations for sperm competition may not always be in Arnqvist G, Edvardsson M, Friberg U, Nilsson T. 2000. Sexual con- the best interests of females. Male seminal fluid proteins can pro - flict promotes speciation in insects. Proc Natl Acad Sci USA. 97: foundly affect female reproductive physiology, promoting rapid 10460–10464. Arnqvist G, Rowe L. 2005. Sexual conflict. New Jersey: Princeton egg deposition and/or inhibiting female sexual receptivity to University Press. rival males (Arnqvist and Rowe 2005). In this way, seminal fluid Gavrilets S. 2000. Rapid evolution of reproductive barriers driven by sexual proteins represent an important weapon in the arsenal of male conflict. Nature. 403:886–889. postmating competition for fertilizations. In some species, semi- Gavrilets S, Waxman D. 2002. Sympatric speciation by sexual conflict. Proc Natl Acad Sci USA. 99:10533–10538. nal fluid proteins are absorbed through the female’s reproduc - Parker GA, Birkhead TR. 2013. Polyandry: the history of a revolution. tive tract and into her blood stream, while in others, the male’s Philos Trans R Soc Lond B Biol Sci. 368:20120335. genitalia can pierce the female’s reproductive tract allowing direct Simmons LW, 2001. Sperm competition and its evolutionary consequences access of seminal fluid to her body cavity. Importantly, seminal in the insects. Princeton: Princeton University Press. fluids that benefit males in postmating sperm competition are Tinghitella RM, Lackey ACR, Martin M, Dijkstra PD, Drury JP, Heathcote R, Keagy J, Scordato ESC, Tyers AM, 2018. On the role of male competi- frequently costly for females (Arnqvist and Rowe 2005). Females tion in speciation: a review and research agenda. Behav Ecol. 29:783–797. can suffer energetic costs associated with reproductive tract Wojcieszek JM, Simmons LW. 2013. Divergence in genital morphology may wound repair, they can be exposed to pathogens during traumatic contribute to mechanical reproductive isolation in a millipede. Ecol Evol. insemination, or seminal fluid proteins can reduce female mating 3:334–343. Downloaded from https://academic.oup.com/beheco/article-abstract/29/4/800/4762157 by Ed 'DeepDyve' Gillespie user on 11 July 2018

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Behavioral EcologyOxford University Press

Published: Dec 19, 2017

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