Low coverage genomic data resolve the population divergence and gene flow history of an Australian rain forest fig wasp

Population divergence and gene flow are key processes in evolution and ecology. Model-based analysis of genome-wide datasets allows discrimination between alternative scenarios for these processes even in non-model taxa. We used two complementary approaches (one based on the blockwise site frequency spectrum (bSFS), the second on the Pairwise Sequentially Markovian Coalescent (PSMC)) to infer the divergence history of a fig wasp, Pleistodontes nigriventris. Pleistodontes nigriventris and its fig tree mutualist Ficus watkinsiana are restricted to rain forest patches along the eastern coast of Australia, and are separated into northern and southern populations by two dry forest corridors (the Burdekin and St. Lawrence Gaps). We generated whole genome sequence data for two haploid males per population and used the bSFS approach to infer the timing of divergence between northern and southern populations of P. nigriventris, and to discriminate between alternative isolation with migration (IM) and instantaneous admixture (ADM) models of post divergence gene flow. Pleistodontes nigriventris has low genetic diversity (π = 0.0008), to our knowledge one of the lowest estimates reported for a sexually reproducing arthropod. We find strongest support for an ADM model in which the two populations diverged ca. 196kya in the late Pleistocene, with almost 25% of northern lineages introduced from the south during an admixture event ca. 57kya. This divergence history is highly concordant with individual population demographies inferred from each pair of haploid males using PSMC. Our analysis illustrates the inferences possible with genome-level data for small population samples of tiny, non-model organisms and adds to a growing body of knowledge on the population structure of Australian rain forest taxa.
Methods
Full methods and additional data summaries (including sampling locations and assembly summary metrics) and all cited references are provided in the Molecular Ecology Journal version of this paper, and also on BioRxiv (BIORXIV/2020/959205). The short read data and assembly for this analysis are deposted in the European Nucleotide Archive, Study PRJEB35527, available from https://www.ebi.ac.uk/ena/browser/view/PRJEB35527

The associated files are scripts and a Mathematica notebook and scripts used for demographic analysis using variants in genome-wide sampling of sequence blocks in an Australian fig wasp, Pleistodontes nigriventris.