Experimental sexual selection affects the evolution of physiological and life‐history traits

Sexual selection and sexual conflict are expected to affect all aspects of the phenotype, not only traits that are directly involved in reproduction. Here, we show coordinated evolution of multiple physiological and life-history traits in response to long-term experimental manipulation of the mating system in populations of Drosophila pseudoobscura. Development time was extended under polyandry relative to monogamy in both sexes, potentially due to higher investment in traits linked to sexual selection and sexual conflict. Individuals (especially males) evolving under polyandry had higher metabolic rates and locomotor activity than those evolving under monogamy. Polyandry individuals also invested more in metabolites associated with increased endurance capacity and efficient energy metabolism and regulation, namely lipids and glycogen. Finally, polyandry males were less desiccation- and starvation resistant than monogamy males, suggesting trade-offs between resistance and sexually selected traits. Our results provide experimental evidence that mating systems can impose selection that influences the evolution of non-sexual phenotypes such as development, activity, metabolism and nutrient homeostasis

Experimental sexual selection affects the evolution of physiological and life?history traits

Sexual selection and sexual conflict are expected to affect all aspects of the phenotype, not only traits that are directly involved in reproduction. Here, we show coordinated evolution of multiple physiological and life-history traits in response to long-term experimental manipulation of the mating system in populations of Drosophila pseudoobscura. Development time was extended under polyandry relative to monogamy in both sexes, potentially due to higher investment in traits linked to sexual selection and sexual conflict. Individuals (especially males) evolving under polyandry had higher metabolic rates and locomotor activity than those evolving under monogamy. Polyandry individuals also invested more in metabolites associated with increased endurance capacity and efficient energy metabolism and regulation, namely lipids and glycogen. Finally, polyandry males were less desiccation- and starvation resistant than monogamy males, suggesting trade-offs between resistance and sexually selected traits. Our results provide experimental evidence that mating systems can impose selection that influences the evolution of non-sexual phenotypes such as development, activity, metabolism and nutrient homeostasis

Data from: Persistent postmating, prezygotic reproductive isolation between populations

Studying reproductive barriers between populations of the same species is critical to understand how speciation may proceed. Growing evidence suggests postmating, prezygotic (PMPZ) reproductive barriers play an important role in the evolution of early taxonomic divergence. However, the contribution of PMPZ isolation to speciation is typically studied between species in which barriers that maintain isolation may not be those that contributed to reduced gene flow between populations. Moreover, in internally fertilizing animals, PMPZ isolation is related to male ejaculate – female reproductive tract incompatibilities but few studies have examined how mating history of the sexes can affect the strength of PMPZ isolation and the extent to which PMPZ isolation is repeatable or restricted to particular interacting genotypes. We addressed these outstanding questions using multiple populations of Drosophila montana. We show a recurrent pattern of PMPZ isolation, with flies from one population exhibiting reproductive incompatibility in crosses with all three other populations, while those three populations were fully fertile with each other. Reproductive incompatibility is due to lack of fertilization and is asymmetrical, affecting female fitness more than males. There was no effect of male or female mating history on reproductive incompatibility, indicating that PMPZ isolation persists between populations. We found no evidence of variability in fertilization outcomes attributable to different female x male genotype interactions, and in combination with our other results, suggests that PMPZ isolation is not driven by idiosyncratic genotype x genotype interactions. Our results show PMPZ isolation as a strong, consistent barrier to gene flow early during speciation and suggest several targets of selection known to affect ejaculate-female reproductive tract interactions within species that may cause this PMPZ isolation

Within-population sperm competition intensity does not predict asymmetry in conpopulation sperm precedence

Postcopulatory sexual selection can generate evolutionary arms races between the sexes resulting in the rapid coevolution of reproductive phenotypes. As traits affecting fertilization success diverge between populations, postmating prezygotic (PMPZ) barriers to gene flow may evolve. Conspecific sperm precedence is a form of PMPZ isolation thought to evolve early during speciation yet has mostly been studied between species. Here, we show conpopulation sperm precedence (CpSP) between Drosophila montana populations. Using Pool-seq genomic data we estimate divergence times and ask whether PMPZ isolation evolved in the face of gene flow. We find models incorporating gene flow fit the data best indicating populations experienced considerable gene flow during divergence. We find CpSP is asymmetric and mirrors asymmetry in non-competitive PMPZ isolation, suggesting these phenomena have a shared mechanism. However, we show asymmetry is unrelated to the strength of postcopulatory sexual selection acting within populations. We tested whether overlapping foreign and coevolved ejaculates within the female reproductive tract altered fertilization success but found no effect. Our results show that neither time since divergence nor sperm competitiveness predicts the strength of PMPZ isolation. We suggest that instead cryptic female choice or mutation-order divergence may drive divergence of postcopulatory phenotypes resulting in PMPZ isolation. This article is part of the theme issue 'Fifty years of sperm competition'

Within-population sperm competition intensity does not predict asymmetry in conpopulation sperm precedence

Funding: M.D.G. was supported by an Adapting to the Challenges of a Changing Environment (ACCE) Doctoral Training Partnership grant no. NE/L002450/1, funded by the Natural Environment Research Council (NERC). L.H.Y. was supported by a studentship funded bythe University of St Andrews and MGR.Postcopulatory sexual selection can generate evolutionary arms races between the sexes resulting in the rapid coevolution of reproductive phenotypes. As traits affecting fertilization success diverge between populations, postmating prezygotic (PMPZ) barriers to gene flow may evolve. Conspecific sperm precedence is a form of PMPZ isolation thought to evolve early during speciation yet has mostly been studied between species. Here, we show conpopulation sperm precedence (CpSP) between Drosophila montana populations. Using Pool-seq genomic data we estimate divergence times and ask whether PMPZ isolation evolved in the face of gene flow. We find models incorporating gene flow fit the data best indicating populations experienced considerable gene flow during divergence. We find CpSP is asymmetric and mirrors asymmetry in non-competitive PMPZ isolation, suggesting these phenomena have a shared mechanism. However, we show asymmetry is unrelated to the strength of postcopulatory sexual selection acting within populations. We tested whether overlapping foreign and coevolved ejaculates within the female reproductive tract altered fertilization success but found no effect. Our results show that neither time since divergence nor sperm competitiveness predicts the strength of PMPZ isolation. We suggest that instead cryptic female choice or mutation-order divergence may drive divergence of postcopulatory phenotypes resulting in PMPZ isolation. This article is part of the theme issue 'Fifty years of sperm competition'.Publisher PDFPeer reviewe

The genetic basis of a recent transition to live-bearing in marine snails

Key innovations are fundamental to biological diversification, but their genetic basis is poorly understood. A recent transition from egg-laying to live-bearing in marine snails (Littorina spp.) provides the opportunity to study the genetic architecture of an innovation that has evolved repeatedly across animals. Individuals do not cluster by reproductive mode in a genome-wide phylogeny, but local genealogical analysis revealed numerous small genomic regions where all live-bearers carry the same core haplotype. Candidate regions show evidence for live-bearer–specific positive selection and are enriched for genes that are differentially expressed between egg-laying and live-bearing reproductive systems. Ages of selective sweeps suggest that live-bearer–specific alleles accumulated over more than 200,000 generations. Our results suggest that new functions evolve through the recruitment of many alleles rather than in a single evolutionary step

Toward the integration of speciation research

Acknowledgements: We thank the staff of the Tvärminne Zoological Station (University of Helsinki) for their hospitality during the workshop. We are also grateful to everyone who applied to attend the workshop.Funder: European Society for Evolutionary Biology; DOI: https://doi.org/10.13039/501100013632Speciation research—the scientific field focused on understanding the origin and diversity of species—has a long and complex history. While relevant to one another, the specific goals and activities of speciation researchers are highly diverse, and scattered across a collection of different perspectives. Thus, our understanding of speciation will benefit from efforts to bridge scientific findings and the diverse people who do the work. In this paper, we outline two ways of integrating speciation research: (i) scientific integration, through the bringing together of ideas, data, and approaches; and (ii) social integration, by creating ways for a diversity of researchers to participate in the scientific process. We then discuss five challenges to integration: (i) the multidisciplinary nature of speciation research, (ii) the complex language of speciation; (iii) a bias toward certain study systems; (iv) the challenges of working across scales; and (v) inconsistent measures and reporting standards. We provide practical steps that individuals and groups can take to help overcome these challenges, and argue that integration is a team effort in which we all have a role to play

Toward the integration of speciation research

Acknowledgements: We thank the staff of the Tvärminne Zoological Station (University of Helsinki) for their hospitality during the workshop. We are also grateful to everyone who applied to attend the workshop.Funder: European Society for Evolutionary Biology; DOI: https://doi.org/10.13039/501100013632Speciation research—the scientific field focused on understanding the origin and diversity of species—has a long and complex history. While relevant to one another, the specific goals and activities of speciation researchers are highly diverse, and scattered across a collection of different perspectives. Thus, our understanding of speciation will benefit from efforts to bridge scientific findings and the diverse people who do the work. In this paper, we outline two ways of integrating speciation research: (i) scientific integration, through the bringing together of ideas, data, and approaches; and (ii) social integration, by creating ways for a diversity of researchers to participate in the scientific process. We then discuss five challenges to integration: (i) the multidisciplinary nature of speciation research, (ii) the complex language of speciation; (iii) a bias toward certain study systems; (iv) the challenges of working across scales; and (v) inconsistent measures and reporting standards. We provide practical steps that individuals and groups can take to help overcome these challenges, and argue that integration is a team effort in which we all have a role to play