Postmating-prezygotic isolation between two allopatric populations of Drosophila montana: fertilisation success differs under sperm competition

Abstract

Postmating but prezygotic (PMPZ) interactions are increasingly recognized as a potentially important early-stage barrier in the evolution of reproductive isolation. A recent study described a potential example between populations of the same species: single matings between Drosophila montana populations resulted in differential fertilisation success because of the inability of sperm from one population (Vancouver) to penetrate the eggs of the other population (Colorado). As the natural mating system of D. montana is polyandrous (females remate rapidly), we set up double matings of all possible crosses between the same populations to test whether competitive effects between ejaculates influence this PMPZ isolation. We measured premating isolation in no-choice tests, female fecundity, fertility and egg-to-adult viability after single and double matings as well as second-male paternity success (P2). Surprisingly, we found no PMPZ reproductive isolation between the two populations under a competitive setting, indicating no difficulty of sperm from Vancouver males to fertilize Colorado eggs after double matings. While there were subtle differences in how P2 changed over time, suggesting that Vancouver males' sperm are somewhat less competitive in a first-male role within Colorado females, these effects did not translate into differences in overall P2. Fertilisation success can thus differ dramatically between competitive and noncompetitive conditions, perhaps because the males that mate second produce higher quality ejaculates in response to sperm competition. We suggest that unlike in more divergent species comparisons, where sperm competition typically increases reproductive isolation, ejaculate tailoring can reduce the potential for PMPZ isolation when recently diverged populations interbreed.

Keywords: Ejaculate tailoring; ejaculate–ejaculate interaction; postcopulatory sexual selection; reproductive isolation; speciation.

Figure 1

Drosophila montana mating pair.

Figure 2

Principal component analysis conducted with 37 SNP markers. Each point represents an individual. Principal component 1 (14.07% of the variance) clearly differentiates the two populations.

Figure 3

Egg‐to‐adult viability after remating in the eight crosses performed. Crosses are abbreviated by female population, 1st male, and 2nd male population, respectively. C, Colorado; V, Vancouver.

Figure 4

Model predictions and 95% confidence intervals from GLMM for P₂ over time in different crosses for Colorado (A) and Vancouver (B) females. Crosses are abbreviated by female population, 1st male, and 2nd male population, respectively. C, Colorado, V, Vancouver.