Abstract

Promiscuity can drive the evolution of sexual conflict before and after mating occurs. Post mating, the male ejaculate can selfishly manipulate female physiology, leading to a chemical arms race between the sexes. Theory suggests that drift and sexually antagonistic coevolution can cause allopatric populations to evolve different chemical interactions between the sexes, thereby leading to postmating reproductive barriers and speciation. There is, however, little empirical evidence supporting this form of speciation. We tested this theory by creating an experimental evolutionary model of Drosophila melanogaster populations undergoing different levels of interlocus sexual conflict. We found that allopatric populations under elevated sexual conflict show assortative mating, indicating premating reproductive isolation. Further, these allopatric populations also show reduced copulation duration and sperm defense ability when mating happens between individuals across populations compared to that within the same population, indicating postmating prezygotic isolation. Sexual conflict can cause reproductive isolation in allopatric populations through the coevolution of chemical (postmating prezygotic) as well as behavioural (premating) interactions between the sexes. Thus, to our knowledge, we provide the first comprehensive evidence of postmating (as well as premating) reproductive isolation due to sexual conflict.

Highlights

  • An alternative to phylogenetic analysis that has been used to directly test the hypothesis is through experimental evolution which follows a simple experimental design: a

  • Males and females used in the assays were either from the same replicate population or from different replicate populations within a regime, which we term as ‘within replicate’ (WR) and ‘between replicate’ (BR) respectively

  • We used experimental evolution to show that high levels of SAC can lead to the evolution of early stages of reproductive isolation at (a) premating and (b) postmating prezygotic stages in populations of Drosophila melanogaster

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Summary

Introduction

An alternative to phylogenetic analysis that has been used to directly test the hypothesis is through experimental evolution which follows a simple experimental design: a. B. Thereafter quantifying RI between allopatric populations within a regime and comparing the extent of isolation between different regimes. Thereafter quantifying RI between allopatric populations within a regime and comparing the extent of isolation between different regimes Following this hypothesis, upon secondary contact, allopatric populations will show relatively stronger evidence of RI in the high conflict regime compared to low/no conflict regime. Martin and Hosken tested this hypothesis in Sepsis cynipsea by evolving replicate populations under polygamy (SAC) and monogamy They found that allopatric pairs showed significantly less mating success compared to their sympatric counterparts in the polygamous, but not in the monogamous, regime; providing the first evidence that antagonistically evolving behavioural traits can lead to reproductive isolation[14]. Despite multiple studies testing the hypothesis in different organisms, the study by Martin and Hosken remains the only direct evidence of SAC as a driver of RI so far[16,17,18,19,20], and the idea of sexual conflict as an ‘engine of speciation’ remains controversial[21]

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