Evidence of linked selection on the Z chromosome of hybridizing hummingbirds*

Abstract

Levels of genetic differentiation vary widely along the genomes of recently diverged species. What processes cause this variation?Here, I analyze geographic population structure and genome-wide patterns of variation in the Rufous, Allen's, and Calliope Hummingbirds (Selasphorus rufus/Selasphorus sasin/Selasphorus calliope) and assess evidence that linked selection on theZ chromosome drives patterns of genetic differentiation in a pair of hybridizing species. Demographic models, introgression tests, and genotype clustering analyses support a reticulate evolutionary history consistent with divergence during the late Pleistocene followed by gene flow across migrant Rufous and Allen's Hummingbirds during the Holocene. Relative genetic differentiation (F st ) is elevated, and within-population diversity (π) is depressed on the Z chromosome in all interspecific comparisons. The ratio of Z to autosomal within-population diversity is much lower than that expected from population size effects alone, and Tajima's D is depressed on the Z chromosome in S. rufus and S. calliope. These results suggest that conserved structural features of the genome play a prominent role in shaping genetic differentiation through the early stages of speciation in northern Selasphorus hummingbirds, and that the Z chromosome is a likely site of genes underlying behavioral and morphological variation in the group.

Genomic differentiation across the speciation continuum in three hummingbird species pairs

“…Our most reproductively-isolated species pair, Calypte had the highest average F ST (Calypte, F ST = 0.323; Archilochus, F ST = 0.112), though Calypte and Archilochus had a qualitatively similar number of F ST peaks. For all three pairs, F ST was higher on the Z chromosome than on the autosomes, with a significant overrepresentation of high-F ST windows on the Z chromosome (Calypte, χ 2 = 40.975, P = 1.27 × 10 − 9 ; Archilochus, χ 2 = 292.91, P = 2.2 × 10 − 16 ; Selasphorus, χ 2 = 674.01, P = 2.2 × 10 − 16 ; Supplemental Table 1), consistent with the findings of Battey [58] in the Selasphorus species pair and Elgvin et al in Passer sparrows [59]. When comparing F ST across chromosome types, Selasphorus, the least-reproductively isolated species pair only had noticeably elevated F ST on the Z chromosome, and not on autosomes, and no significant difference in number of elevated F ST peaks on microchromosomes versus macrochromosomes (χ 2 = 0.09577, P = 0.757).…”

“…High linkage on macrochromosomes results in reduced diversity which leads to the accumulation of F ST peaks on macrochromosomes observed at later stages of speciation. Elevated F ST windows were especially common on the Z chromosome in all three species, as expected based on prior work in hummingbirds [58] and other taxa [42]. The large X-effect, or the observation that sex chromosomes play a disproportionate role in speciation, is thought to be the overarching cause of the commonly found pattern of elevated F ST on sex chromosomes relative to autosomes.…”

Robbery in progress: Historical museum collections bring to light a mitochondrial capture within a bird species widespread across southern Australia, the Copperback Quail‐thrush Cinclosoma clarum

“…Recently, sometimes unexpected complexity of sex chromosome markers has been highlighted ( cf . Lasne, van Heerwaarden, Sgrò, & Connallon, 2018; Battey, 2020; Hayes, Barton, & Zeng, 2020). This system offers much to the study of the genomics of differentiation and speciation.…”

The population genetics of nonmigratory Allen’s Hummingbird (Selasphorus sasin sedentarius) following a recent mainland colonization

“…While Godwin et al. (2020) analyzed the broader patterns of gene flow and divergence across Allen's Hummingbird (both subspecies) and Battey (2020) included both subspecies of Allen's as well as Rufous ( S. rufus ) Hummingbird, the present study explicitly focuses on the island–mainland colonization dynamics of nonmigratory Allen's Hummingbird.…”