Abstract
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’.
Highlights
Widespread polyandry in animals presents the opportunity for postcopulatory sexual selection and sexual antagonism to accelerate the coevolution of male ejaculate × female reproductive tract interactions [1,2,3,4,5]
If postcopulatory sexual selection can facilitate the evolution of postmating prezygotic (PMPZ) isolation, asymmetries in the strength of PMPZ isolation acting between taxa may reflect differences in the strength of sexual selection acting within populations
We tested the prediction that PMPZ isolation asymmetries would reflect differences in the intensity of postcopulatory sexual selection acting within populations [16] by measuring two common proxies for the intensity of sperm competition faced by males: male reproductive mass investment and sequential mating capacity [40,41,42]
Summary
Widespread polyandry in animals presents the opportunity for postcopulatory sexual selection (sperm competition and cryptic female choice) and sexual antagonism to accelerate the coevolution of male ejaculate × female reproductive tract interactions [1,2,3,4,5]. The appearance of isolating mechanisms should reduce gene flow during or following divergence, but the demographic histories of taxa in studies of CpSP are often poorly resolved, hampering inference about the time scale and role of CpSP in nascent reproductive isolation. It is not currently known whether CpSP can evolve during divergence with extensive gene flow or such incompatibilities only appear or spread after gene flow has ceased. Using the D. montana system, we set out to ask (i) what is the relative time scale of divergence and is there evidence for gene flow during divergence? And more recently, (ii) do populations show CpSP and if so, is it concordant with non-competitive 2 PMPZ isolation? (iii) Is the strength of PMPZ isolation predicted by the strength of postcopulatory sexual selection acting within populations? And (iv), do overlapping foreign and coevolved ejaculates interact to alter PMPZ outcomes?
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