Modeling the Multiple Facets of Speciation-with-Gene-Flow Towards Inferring the Divergence History of Lake Whitefish Species Pairs (Coregonus Clupeaformis)

Abstract

AbstractParallel divergence patterns across replicated species pairs occurring in similar environmental contrasts may arise through distinct evolutionary scenarios. Deciphering whether such parallelism actually reflects repeated parallel divergence driven by divergent selection or a single divergence event with subsequent gene flow needs to be ascertained. Reconstructing historical gene flow is therefore of fundamental interest to understand how demography and selection jointly shaped genomic divergence during speciation. Here, we use an extended modeling framework to explore the multiple facets of speciation-with-gene-flow with demo-genetic divergence models that capture both temporal and genomic variation in effective population size and migration rate. We investigate the divergence history of five sympatric Lake Whitefish limnetic (dwarf) and benthic (normal) species pairs characterized by variable degrees of ecological divergence and reproductive isolation. Genome-wide SNPs were used to document the extent of genetic differentiation in each species pair, and 26 divergence models were fitted and compared to the unfolded joint allele frequency spectrum of each pair. We found evidence that a recent (circa 3000-4000 generations) asymmetrical secondary contact between expanding post-glacial populations has accompanied Whitefish diversification. Our results suggest that heterogeneous genomic differentiation patterns have emerged through the combined effects of linked selection generating variable rates of lineage sorting across the genome during geographical isolation, and heterogeneous introgression eroding divergence at different rates across the genome upon secondary contact. This study thus provides a new retrospective insight into the historical demographic and selective processes that shaped a continuum of divergence associated with ecological speciation.