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.

Speciation and secondary contact in a fossorial island endemic, the São Tomé caecilian

“…Our study joins a growing number of systems demonstrating speciation at small spatial scales on islands (Bourgeois et al, 2020; Gabrielli et al, 2020; Heaney et al, 2018; Kisel & Barraclough, 2010; Osborne et al, 2020; Savolainen et al, 2006). We propose that transient geographic barriers coupled with local adaption across environmental gradients can contribute to the accumulation of phenotypic and taxonomic diversity.…”

Within-island diversification in a passerine bird

“…Reunion and Mauritius are 170 km apart; both islands emerged from the ocean floor at a depth of 4.5-5 km, and were, therefore, never connected to each other [66]. While we did not specifically estimate migration rates, our phylogenetic data and previous work [67] suggest that gene flow between Reunion and Mauritius grey white-eyes is absent or very low and, if any, has clearly not prevented population divergence (F ST estimate of 0.18) (electronic supplementary material, figure S10; see also [37,38]). Our results also indicate that geographical differentiation has not been followed by secondary colonizations between islands, highlighting the role of inter-island colonization in the global diversification of white-eyes [26] and, more generally, the build-up of species diversity on oceanic archipelagos [11,68].…”

“…Recent studies have shown that more variation exists among the different geographical forms of the Reunion grey white-eye than would be expected under drift for both morphological and plumage colour traits [34,42]. Thus, while geographical isolation may have promoted evolutionary divergence between all forms, sexual selection also appears to have played a major role in the establishment of reproductive isolation [37]. Range expansion followed by range splitting or dispersal across the elevational gradient that led to the formation of the highland form seems to have been key in promoting ecological diversification within the lineage, with divergent selection pressures causing at least adaptive divergence and possibly also contributing to reproductive isolation [37,42,78].…”

“…[6]). Recent studies, however, have shown that the Reunion grey white-eye consists of four distinct adjacent and non-overlapping geographical forms that exhibit discrete differences in morphology and plumage (electronic supplementary material, text S1) and form extremely narrow hybrid zones where they meet [33][34][35][36][37]. Three of the geographical forms are found in the lowlands, primarily below 1400 m, with contact zones coinciding with natural physical barriers, such as large rivers or lava flows, that are not associated with changes in environmental conditions [36].…”

“…This highland form occupies a distinct elevational and ecological zone [40,41], suggesting that it may have experienced very different selection pressures during its evolutionary history. This may explain at least partly why it is phenotypically and genetically different from the lowland forms [37,38,42]. Such disparity could have arisen as a result of the ecological and evolutionary expansion of a lineage to exploit new resource types, providing a possible case of adaptive divergence structured by elevation.…”