Selection on a novel locus and Pleistocene glaciations explain plumage patterning evolution in the Rufous-collared Sparrow (Zonotrichia capensis)

LAVINIA, PABLO D.; CAMPAGNA, LEONARDO; BARREIRA, ANA S.; LOUGHEED, STEPHEN C.; TUBARO, PABLO L.; LIJTMAER, DARÍO A.

Congreso; Evolution 2021; 2021

Society for the Study of Evolution (SSE)

The Rufous-collared Sparrow (Zonotrichia capensis) shows phenotypic variation throughout its distribution. In particular, subspecies australis from southern Chile and Argentina differentiates from other subspecies by lacking the characteristic black lateral crownstripes. We sequenced whole genomes of 18 individuals (9 representing australis and 9 from northcentral Argentina) to investigate the genomic changes behind this phenotypic differentiation. Based on the analysis of ~ 11 million SNPs, we detected one main divergence peak (FST = 0.26 ± 0.35) on scaffold 42 that contrast with a background of low genomic differentiation (FST = 0.015 ± 0.018) between australis and the other individuals. This ~465-kb region, which concentrates 90% of outlier SNPs and virtually all fixed differences across genome, was mapped to chromosome 5. Outlier SNPs were concentrated within and downstream the Suppression of tumorigenicity 5 gene (ST5), also known as DENN2B. This gene regulates RAB9A, which is required for melanosome biogenesis and melanocyte pigmentation in mammals, making it a candidate gene for melanic plumage polymorphism within Z. capensis. Differences at ST5 could be responsible for the uniformly grey head of australis, subspecies in which all other black plumage patches are also paler or less prominent. Our results also indicated that this genomic island of differentiation formed as a result of background and/or purifying selection acting on allopatric populations, with selection against gene flow at this locus also occurring at some degree. Mitochondrial DNA indicated that australis diverged from other subspecies round 400,000 years ago. Taken together, our study suggests that australis populations became isolated in Patagonia during Pleistocene glaciations and diverged in situ in one or more refuges. Phenotypic differences would have evolved rapidly during this isolation period. Then, after the retreat of the ice sheets, the isolated populations would have become into contact and resumed gene flow, homogenizing nuclear but not mitochondrial DNA.