Ready, set, speciate: The role of sex chromosomes in the divergence of Reunion grey white-eye morphs

Genomic analyses find evidence for sex-linked diversification of island populations.

Sex chromosomes can drive speciation. From a genetic point of view, the origin of new species can be seen as the slow accumulation of genetic mismatches – so-called Bateson-Dobzhansky-Muller incompatibilities – between populations. These genetic mismatches often arise on sex chromosomes for several reasons (reviewed by Darren Irwin in this excellent paper). For example, important reproductive isolation mechanisms, such as male sterility, male plumage traits, and assortative mating, have all been linked to sex chromosomes. If these chromosomes are involved in the build-up of reproductive isolation, you expect genomic regions on the sex chromosomes to be more divergent compared to other chromosomes (i.e. the autosomes). A recent study in the journal Molecular Ecology tested this idea for the Reunion grey white-eye (Zosterops borbonicus).

Zosterops borbonicus

The Reunion grey white-eye © David Monniaux | Wikimedia Commons

 

Color Morphs

I have written about the Reunion grey white-eye before (see this blog post from 2017). On the small island of Reunion, this small passerine occurs in several populations with distinct plumage patterns. In the lower parts of the island, you can find a brown-headed brown (BHB), a grey-headed brown (GHB), and a brown-naped brown form (BNB). A fourth form is restricted to the highlands (between 1,400 and 3,000 m) and comprises two very distinct color morphs. Previous genetic work uncovered narrow hybrid zones between several populations and suggested that these color morphs are separated by a few genomic regions. Unfortunately, the resolution of genetic markers (microsatellites) was too weak to pinpoint the exact genomic regions that might be involved in reproductive isolation. Recently, Yann Bourgeois and his colleagues used genomic data to fill this gap in our knowledge on the Reunion grey white-eye.

reunion_map

A map of Reunion showing the different Zosterops populations. From: Bourgeois et al. (2020) Molecular Ecology

 

Sex-linked Genes

The results were in line with an important role for sex chromosomes in the early stages of speciation on Reunion. First, the autosomal markers could only discriminate between lowland and highland populations, whereas the sex-linked markers uncovered more fine-grained population structure within the lowland morphs. Second, the researchers contrasted demographic models with autosomal and sex-linked markers. The models with sex-linked markers pointed to lower levels of gene flow between the different populations compared to models based on autosomal markers. This suggests that some genomic regions on the sex chromosomes are not being exchanged between the populations and might harbor genes involved in reproductive isolation.

To identify candidate genes for reproductive isolation, the researchers searched the genomes for divergent regions. These analyses uncovered several promising genomic locations, including a clear outlier on chromosome 4A. Wait a minute, you might say, chromosome 4A is not a sex chromosome! Well, recent studies reported the existence of special sex chromomes in the Sylvioidea superfamily, to which the Reunion grey white-eye belongs. Several genomic locations – including part of chromosome 4A – have fused with fused with the existing sex chromosomes, giving rise to neo-sex chromosomes (you can read the entire story in this blog post).

genomic_landscape

Scanning the genomes of the white-eyes for divergent regions uncovered a clear peak on chromosome 4A, which has fused with the traditional sex chromosome. From: Bourgeois et al. (2020) Molecular Ecology

 

Plumage Patterns

Additional analyses revealed two interesting candidate genes that are involved in plumage coloration: TYRP1 and WNT5A. Interestingly, WNT5A is known to regulate the expression of TYRP1. These findings “suggests that a large part of plumage colour variation between the geographical forms of the Reunion grey white-eye may be controlled by a set of a few loci of major effect. More detailed studies of hybrid zones between the different lowland forms may help to characterize the exact association of alleles that produce a given plumage color phenotype.” Other studies have already taken advantage of hybrid zones to pinpoint specific plumage genes, such crows and warblers. Hopefully, the Reunion grey white-eye can be a new addition to this list.

 

References

Bourgeois, Y. X., Bertrand, J. A., Delahaie, B., Holota, H., Thébaud, C., & Milá, B. (2020). Differential divergence in autosomes and sex chromosomes is associated with intra‐island diversification at a very small spatial scale in a songbird lineage. Molecular Ecology29(6), 1137-1153.

 

This paper has been added to the Zosteropidae page.

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