Reproductive Isolation through Experimental Manipulation of Sexually Antagonistic Coevolution in Drosophila 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.

The Past and Future of Experimental Speciation

“…Subsequent work on sexual selection and speciation continues to fail to find significant RI [14][15][16][17], even when manipulating genetic variation and population size to increase the likelihood of response [14] and assessing different RI barriers [15]. One species, Drosophila melanogaster, has been tested independently in two laboratories but only one study found RI [18,19]. Theory suggests that different components of sexual selection may interfere with the evolution of RI [20] and one ES study supports this interpretation.…”

“…Previous ES studies focused on premating barriers using patterns of assortative mating to measure RI [29]. Although this remains true for ES studies post-Fry [16,24,27,[30][31][32][33][34], some have included postmating, prezygotic [18,32,35], and postzygotic [24,[36][37][38] forms of RI. However, more ES studies comparing the speed of evolution, the traits targeted, and relative magnitude of extrinsic and intrinsic RI are necessary to understand mechanisms by which RI evolves.…”

Absence of reproduction-immunity trade-off in male Drosophila melanogaster evolving under differential sexual selection

“…Nongenetic parental effects [48]can lead to misinterpretation of multi-generation selection experiment results. To equalize such effects across selection regimes, all selected populations were passed through one generation of standardization where selection was removed, i.e., they were maintained in ancestral conditions [49]. Adult progeny produced by this generation were used for the experiment.…”

Absence of reproduction-immunity trade-off in male Drosophila melanogaster evolving under differential sexual selection

“…Nongenetic parental effects [48]can lead to misinterpretation of multi-generation selection experiment results. To equalize such effects across selection regimes, all selected populations were passed through one generation of standardization where selection was removed, i.e., they were maintained in ancestral conditions [49]. Adult progeny produced by this generation were used for the experiment.…”