Geographic patterns of postzygotic isolation between two closely related widespread dung fly species (Sepsis cynipseaandSepsis neocynipsea; Diptera: Sepsidae)

Abstract

Identifying the contribution of pre‐ and postzygotic barriers to gene flow is a key goal of speciation research. The widespread dung fly species Sepsis cynipsea and Sepsis neocynipsea offer great potential for studying the speciation process over a range of opportunities for gene exchange within and across sister species (cross‐continental allopatry, continental parapatry and sympatry). We examined the role of postcopulatory isolating barriers by comparing female fecundity and egg‐to‐adult viability of F1 and F2 hybrids, as well as backcrosses of F1 hybrids with the parental species, via replicated crosses of sym‐, para‐ and allopatric populations. Egg‐to‐adult viability was strongly but not totally suppressed in hybrids, and offspring production approached nil in the F2 generation (hybrid breakdown), indicating yet unspecified intrinsic incompatibilities. Viable F1 hybrid offspring showed almost absolute male (the heterogametic sex) sterility while females remained largely fertile, in accordance with Haldane's rule. Hybridization between the two species in European areas of sympatry (Swiss Alps) indicated only minor reinforcement based on fecundity traits. Crossing geographically isolated European and North American S. neocynipsea showed similar albeit weaker isolating barriers that are most easily explained by random genetic drift. We conclude that in this system with a biogeographic continuum of reproductive barriers, speciation is mediated primarily by genetic drift following dispersal of flies over a wide (allopatric) geographic range, with some role of natural or sexual selection in incidental or direct reinforcement of incompatibility mechanisms in areas of European sympatry. S(ubs)pecies status of continental S. neocynipsea appears warranted.

Exaggerated male forelegs are not more differentiated than wing morphology in two widespread sister species of black scavenger flies

“…Most crucially, however, our study does not support the often-raised prediction that sexually selected traits (here the male foreleg) evolve faster than naturally selected traits (here the wing; Arnqvist, 1998;Arnqvist & Rowe, 2005). Given that all investigated European S. neocynipsea populations are sympatric with S. cynipsea, we additionally detected slightly stronger fore femur differentiation in sympatry versus cross-continental allopatry (presumably due to character displacement: Giesen et al, 2017;Giesen et al, 2019). Whether sexual selection acts not only on the male forelegs but perhaps also the male wings remains to be directly assessed.…”

“…Sexual selection is considered an important evolutionary force that may not only lead to rapid trait diversification, but also promotes population differentiation and speciation (Arnqvist & Rowe, ; Hosken & Stockley, ). Our quantitative genetic breeding design uncovered significant differentiation in fore femur shape among the two closely related sister species, as well as between the continental populations of S. neocynipsea , which are likely undergoing incipient speciation in allopatry (Giesen et al, , ). However, the differentiation of femur morphology was of similar magnitude as that of wing vein positioning, which refutes our original prediction that male ornaments evolve at a higher rate than wings.…”

Temporal niche partitioning of Swiss black scavenger flies in relation to season and substrate age (Diptera, Sepsidae)

“…Rohner et al 2015, Rohner 2015, Rohner and Bächli 2016. These two species hybridize readily in the laboratory, though hybridization is apparently prevented in nature by behavioural incompatibility (Giesen et al 2017(Giesen et al , 2018. Rohner et al (2015) demonstrated greater sepsid species richness at higher altitudes in the Swiss Alps.…”

Genomic signals of admixture and reinforcement between two closely related species of European sepsid flies

“…Previous studies showed that S. cynipsea and S. neocynipsea produce fertile hybrid offspring under laboratory conditions despite strong pre-and postmating isolating barriers. These barriers are mediated by assortative mating behaviors that are partly reinforced in areas where the two species occur in sympatry (Giesen et al, 2017(Giesen et al, , 2019.…”

“…In contrast, less gene flow in sympatry than in allopatry would indicate selection against gene flow and thus suggest reinforcement of reproductive barriers at sites of co-occurrence (Butlin, 1995;Noor, 1999;Coyne & Orr, 2004;e.g. Kulathinal & Singh, 2000;Massie & Makow, 2005;Giesen et al 2017Giesen et al , 2019.…”