Differential divergence in autosomes and sex chromosomes is associated with intra-island diversification at a very small spatial scale in a songbird lineage.

Abstract

Recently diverged taxa showing marked phenotypic and ecological diversity provide optimal systems to understand the genetic processes underlying speciation. We used genome-wide markers to investigate the diversification of the Reunion grey white-eye (Zosterops borbonicus) on the small volcanic island of Reunion (Mascarene archipelago), where this species complex exhibits four geographical forms that are parapatrically distributed across the island and differ strikingly in plumage colour. One form restricted to the highlands is separated by a steep ecological gradient from three distinct lowland forms which meet at narrow hybrid zones that are not associated with environmental variables. Analyses of genomic variation based on single nucleotide polymorphism data from genotyping-by-sequencing and pooled RAD-seq approaches show that signatures of selection associated with elevation can be found at multiple regions across the genome, whereas most loci associated with the lowland forms are located on the Z sex chromosome. We identified TYRP1, a Z-linked colour gene, as a likely candidate locus underlying colour variation among lowland forms. Tests of demographic models revealed that highland and lowland forms diverged in the presence of gene flow, and divergence has progressed as gene flow was restricted by selection at loci across the genome. This system holds promise for investigating how adaptation and reproductive isolation shape the genomic landscape of divergence at multiple stages of the speciation process.