Rapid, complete reproductive isolation in two closely relatedZosteropsWhite‐eye bird species despite broadly overlapping ranges*

Abstract

Examining what happens when two closely related species come into secondary contact provides insight into the later stages of the speciation process. The Zosteropidae family of birds is one of the most rapidly speciating vertebrate lineages. Members of this family are highly vagile and geographically widespread, raising the question of how divergence can occur if populations can easily come into secondary contact. On the small island of Kolombangara, two closely related nonsister species of white‐eyes, Zosterops kulambangrae and Zosterops murphyi, are distributed along an elevational gradient and come into secondary contact at mid‐elevations. We captured 134 individuals of both species along two elevational transects. Using genotyping‐by‐sequencing data and a mitochondrial marker, we found no evidence of past hybridization events and strong persistence of species boundaries, even though the species have only been diverging for approximately 2 million years. We explore potential reproductive barriers that allow the two species to coexist in sympatry, including premating isolation based on divergence in plumage and song. We also conducted a literature review to determine the time it takes to evolve complete reproductive isolation in congeneric avian species/subspecies in secondary contact (restricted to cases where congeneric taxa are parapatric or have a hybrid zone), finding our study is one of the youngest examples of complete reproductive isolation studied in a genomic context reported in birds.

Gene flow and rapid differentiation characterize a rapid insular radiation in the southwest Pacific (Aves:Zosterops)

“…Despite disagreement about the direction of gene flow, most analyses supported some degree of admixture between these two nonsister species. In contrast, a recent analysis of gene flow and divergence between these two species found complete reproductive isolation and no evidence for gene flow (Cowles and Uy 2019). This difference in results is surprising and could be caused by several differences in study design.…”

Within-island diversification in a passerine bird

“…In fact, across all islands currently occupied by more than one Zosterops species, separate colonizations can be easily invoked (see e.g. [29][30][31][32]). This suggests that in most species, low dispersal ability mainly corresponds to low 'over-water' dispersal.…”

“…White-eyes (Zosteropidae) stand out as a lineage in which diversification rates have been exceptionally high, and with nearly half of the world's forms being single-island endemics, they appear to respond rapidly to the geographical drivers of speciation [26][27][28]. A number of islands are occupied by more than one recognized species, but the presence of multiple species on a single island has been attributed to multiple colonizations in all cases [6,[29][30][31][32]. Uniquely among whiteeyes, and even among birds in general, the Reunion grey white-eye displays geographical variation in morphological and plumage colour traits within the small and remote volcanic oceanic island of Reunion (2512 km 2 ) [33].…”

A comprehensive molecular phylogeny of Afrotropical white-eyes (Aves: Zosteropidae) highlights prior underestimation of mainland diversity and complex colonisation history

“…For example, issues such as introgression are commonly documented between young species, particularly in areas where there is higher sympatry or parapatry between taxa, as a result of selection, and drift (Ballard and Whitlock, 2004). Hybridisation is a common phenomenon in birds (Ottenburghs et al, 2015), with several studies having documented hybridisation between Zosterops subspecies (Milá et al, 2010;Oatley et al, 2017;Oatley et al, 2012), although a recent study of two broadly overlapping young non-sister Zosterops species did not show any evidence of past hybridization events (Cowles and Uy, 2019). Although Bayesian implementation of the GMYC has advantages over the original GMYC model, there are also caveats regarding bGMYC and its performance in identifing species that have recently diverged or clades undergoing rapid radiation (Reid and Carstens, 2012), which is likely the case for some of the taxa within this study (see Appendix A).…”