Patterns of Genomic Divergence
Differentiation between S. v. virens and S. v. waynei was most pronounced in two regions of the genome, one along chromosome 6 and the other on the Z chromosome (Figure 3). Baiz et al., (2021) compared patterns of differentiation between nine sister species across theSetophaga genus. Notably, these regions on chromosome 6 and the Z are also commonly differentiated between several other warbler pairs. However, in those instances, regions of divergence are much larger, on the scale of 1-2 Mb, whereas in the present case the divergent regions are an order of magnitude smaller. We suggest this is likely because all pairs in Baiz et al., (2021) are between fully reproductively isolated species, each sharing a common ancestor much older than that betweenS. v. virens and S. v. waynei . Thus, divergence between those pairs have had more time to accrue greater differences in their genomes. Additionally, this study adds to the number of examples in birds where the Z chromosome is highlighted as highly divergent between related taxa, beyond expectations of a reduced effective population size (Ellegren, 2011; Oyler-McCance et al., 2015; Ruegg et al., 2014).
​​Because the regions of divergence between S. v. virens andS. v. waynei are small, we can identify individual genes within them that were potentially the target of divergent selection between the subspecies. Although the two regions—on chromosome 6 and the Z chromosome—include multiple genes, we focused on two that directly intersected the two most divergent 10Kb windows. In the chromosome 6 region, the gene that intersects the most divergent window is broad substrate specificity ATP-binding cassette transporter ABCG2 isoform X1 (ABCG2; NCBI reference XP_030131844.2). ABCG2 is involved in protein transport, extra- and intra-cellularly (Ma et al., 2020), and recently implicated in egg coloration differences in mallard ducks (Anas platyrhynchos; Liu et al., 2021). The most divergent window within the entire genome, on the Z chromosome, falls within the gene Metallo-Beta-Lactamase Domain Containing 2 (MBLAC2 ). The MBL superfamily of enzymes has a diverse phenotypic role but has been associated with hydrolase activity (Malgapo et al., 2021). While we do not know the function of these genes in warblers, they are both involved in metabolic processes and cellular transport and present a possible connection to the distinct habitat (and therefore diet) these warblers inhabit. Both are good candidates for further study of the implications of gene functionality in birds.
More broadly, the overall limited genomic differentiation suggests these warblers are in the early stages of divergence. Previous studies of closely related avian taxa have commonly identified shared divergence peaks between independent groups (Delmore et al., 2015; Toews, Campagna, et al., 2016). These have generally been understood as genomic regions of reduced recombination, which amplify the influence of divergence via linked selection. However, given the large size and many genes that fall within these regions in previous studies, pinpointing putative targets of selection has been challenging. In the S. v. virens complex, however, the small size of these divergent regions has allowed us to identify ABCG2 and MBLAC2 as two possible targets, and it will be important to understand whether these specific genes have contributed to common divergence patterns in other species pairs.