Extreme sex chromosome differentiation, likely driven by inversion, contrasts with mitochondrial paraphyly between species of crowned sparrows

Abstract

Sympatric species pairs provide researchers with the opportunity to study patterns of genomic differentiation during the late stages of speciation and to identify the genomic regions underlying reproductive isolation. The Golden-crowned Sparrow (Zonotrichia atricapilla) and the White-crowned Sparrow (Zonotrichia leucophrys) are broadly sympatric songbirds found in western North America. These sister species are phenotypically differentiated and largely reproductively isolated despite possessing similar mitochondrial genomes, likely due to recent mitochondrial introgression. We used a genotyping-by-sequencing (GBS) approach to determine the structure of nuclear genomic differentiation between these species and also between two hybridizing subspecies of Z. leucophrys, across more than 45,000 single nucleotide polymorphisms (SNPs). The two Z. leucophrys subspecies showed moderate levels of relative differentiation, as well as patterns consistent with a history of recurrent selection in both ancestral and daughter populations. Z. leucophrys and Z. atricapilla show high levels of relative differentiation and strong heterogeneity in the level of differentiation among different chromosomal regions, with a large portion of the Z chromosome showing highly elevated differentiation. Patterns of relative and absolute differentiation and linkage disequilibrium suggest a large inversion on the Z chromosome, with inversion haplotypes that segregate between Z. atricapilla and Z. leucophrys. While mitochondrial DNA differentiation is often emphasized in studies of speciation, differentiation between these Zonotrichia sparrows appears to have occurred first in the Z chromosome and secondarily in autosomes, followed by mitochondrial introgression. This putative inversion has implications for reproductive isolation between these species and adds to a growing body of evidence for the importance of inversions and the Z chromosome in speciation.