Speciation in the Réunion grey white-eye (Zosterops borbonicus)

During my PhD, I investigated the causes of a striking case of plumage color variation in an island endemic bird: the Réunion grey white-eye (Zosterops borbonicus). This possible case of incipient speciation stands out as one of the very few exceptions of evolutionary divergence documented at the scale of a so small island in birds.

Geographic distribution of the different forms of Z. borbonicus. Three forms occur in parapatry in the lowlands (< 1400 a.s.l.) and another one lives in the highlands where two morphs coexist. (Illustration retrieved from my thesis)

Geographic distribution of the different forms of Z. borbonicus. Three forms display parapatric distributions in the lowlands (< 1400 m a.s.l.) whereas a fourth one occurs in the highlands of Réunion where two morphs coexist. (Illustration from my PhD thesis)

On the evolutionary history of these birds

The Grey Headed Browned-Napped form occurs in the Southern lowlands of Réunion Island (Photo Joris Bertrand)

The Grey Headed Browned-Napped form occurs in the Southern lowlands of Réunion Island (Photo Joris Bertrand)

The first phylogenetic hypothesis (Warren et al., 2006) and population genetic surveys (Milá et al., 2010) supported a scenario of within-island evolutionary divergence with Z. borbonicus being reproductively isolated for a long time (about 400,000 years) from its sister species (Z. mauritianus) which lives on the neighbor island of Mauritius.

On the factors responsible for this small-scale evolutionary divergence

Réunion has been shaped by an intense volcanic activity that gave rise to a rugged topology and ecologically diverse habitats. This has definitely affected the spatial distribution and the demographical dynamics of white-eyes populations. We showed that adaptation to local environmental conditions shape body size and is partly responsible for the restriction in gene flow between populations occurring along an elevational gradient on the West-coast of the island (Bertrand et al., 2016). Along these slopes, we also confirmed the existence of a cryptic hybrid zone between two genetically differentiated highland and lowland forms. We could also verify that the contact zones between the lowland colour forms match physical discontinuities but are not necessarily associated with significant habitat changes and are not corroborated by neutral genetic differentiation (Delahaie et al., in press). It suggests that additional factors related to sexual selection and/or genetic incompatibilities could explain the geographic structure observed. Anyway, only a very particular combination of divergent selective pressures (Cornuault et al., 2015) coupled with a limited propensity to disperse (Bertrand et al., 2014) is able to explain the emergence and the maintenance of these differences. 

On the genetic bases of plumage color

Sympatric brown and grey morphs of the sympatric polymorphic upland form of Z. borbonicus (Photo Joris Bertrand)

Sympatric brown and grey morphs of the sympatric polymorphic upland form of Z. borbonicus (Photo Joris Bertrand)

In these birds, color differences are genetically determined by the deposition of two melanic pigments when the feather grows: the eumelanin (grey) and the pheomelanin (brown). In order to determine the genetic bases of colour variation, we first carried on a ‘candidate gene’ approach by sequencing several genes from the melanocortin’s biosynthesis pathway that are known to be involved in color variation. We found no mutation(s) that could explain colour differences in any of these genes (Bourgeois et al., 2012; 2016). The team therefore applied different protocols to work at the genome scale (Bourgeois et al., 2013). Thanks to these genomic approaches, we could identify a new genomic region undepinning the plumage colour variation we observed (Bourgeois et al., 2017).