Speciation and the processes that establish barriers to gene flow among diverging populations are central to evolutionary biology. Speciation research has largely focused on post hoc testing of evolutionary hypotheses in species with established divergence or on investigating genetic and phenotypic divergence on a microevolutionary scale. Moreover, few empirical studies (e.g. in bacteria, fruit flies) have used integrative and/or systematic approaches to demonstrate isolating mechanisms that can lead to speciation, and even less so in non-model species. Here we use a widespread dung fly species, Sepsis punctum, to investigate how rapid evolution of divergences among allopatric populations in North America and Europe result in reproductive isolation and barriers to gene flow that drive incipient speciation. We take an integrative approach that combines diverse datasets from S. punctum, including population genomics, DNA barcoding, reproductive transcriptomics, novel gene evolution, and genetic variant analysis. In conjunction, we perform evolutionary hypotheses testing in an experimental framework using population crosses to evaluate the role of reproductive traits. We find that S. punctum is in the process of rapidly accumulating reproductive and molecular divergences at the population level, likely driven by a range of behavioural, reproductive, and seminal fluid incompatibilities. These pre-mating and post-mating pre-zygotic (PMPZ) reproductive barriers occur asymmetrically and at varying degrees among population crosses, thereby producing differentials in gene flow and reproductive isolation that underpin incipient speciation in S. punctum.
Asymmetric reproductive isolation and differential gene flow drive incipient speciation in allopatric populations of dung flies