Reproductive Isolation through Experimental Manipulation of Sexually Antagonistic Coevolution inDrosophila melanogaster

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.In sexually reproducing species, males and females often have differential reproductive investment, and, consequently differential evolutionary interest in the outcome of sexual interactions 1, 2 . This often leads to a scenario where adaptations benefitting one sex come at the expense of the other [3][4][5] , bringing about a coevolutionary chase typically called sexually antagonistic coevolution (SAC) 6 . According to verbal 7, 8 and formal 9, 10 arguments, SAC can lead to a perpetual arms race between males and females of the same species. A byproduct of this is the continual divergence between allopatric populations in genes related to reproduction, leading to reproductive isolation (RI) even in the absence of natural selection. This hypothesis is supported indirectly by comparative studies that showed higher rates of speciation in insect clades where sexual conflict is observed than those where it is not observed 11 . However, no such evidence has been found in other studies on mammals, butterflies, spiders 12 and birds 13. 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. Evolving independent replicate (i.e., allopatric) populations maintained under high and low/no conflict regimes (e.g., by enforcing monogamy or altering sex ratio) while all else remains equal. b. 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 ...