Population Genetic Structure of Early-Stage Parapatric Ecological Speciation in the Atlantic Song Sparrow

Abstract

The most basic model of speciation requires two main components: divergent natural selection and isolation. But how does natural selection facilitate the rise of new species without isolation? If a species occupies different habitats across its range, then parapatric (i.e. adjacent) populations can be exposed to divergent selection, possibly leading to speciation. The song sparrow (Passerellidae: Melospiza melodia) is a common songbird with a variety of subspecies found across North America. One subspecies, the Atlantic song sparrow (M. m. atlantica), is a habitat specialist found in the dunes and saltmarshes of the east coast. We investigated the genetic differences of this subspecies from parapatric populations of the eastern song sparrow (M. m. melodia), a widespread generalist. Ecologically-driven parapatric divergence is a fundamental mechanism of speciation, but previous studies have had difficulty characterizing parapatric divergence at the genomic level due to limitations in resolution. We used a contemporary genomic method, RADseq, in conjunction with an assay of a mitochondrial gene to assess how the genomic differentiation of these divergently-adapted, parapatric subspecies have been shaped by ecological selection. We found that a putatively neutral genetic marker did not exhibit divergence between the subspecies, which suggests that they may interbreed frequently in their contact zone and/or have not been reproductively isolated for long enough for divergence to occur, as would be expected in the early stages of parapatric divergence. Analysis of RADmarkers revealed a clinal relationship in the proportion of genetic ancestry assignment with what appears to be extensive intergradation in transitional habitats, which may be due to hybrid superiority or an influx of genes from both parental types in these habitats. These patterns are consistent with our current understanding of parapatric ecological divergence and provide a framework for further investigations into the genomics of ecological speciation.