The contemporary Pacific gray whale ( Eschrichtius robustus ) gene pool includes ancestry from a potential ghost population: inferences from population genomics

Abstract

Local extirpations and extreme bottlenecks can deplete genetic variation and obscure population dynamics, especially in highly mobile species. The gray whale (Eschrichtius robustus) undertakes some of the longest known migrations among mammals, and two stocks (eastern and western gray whales) were historically recognized in the Pacific. Commercial whaling depleted both stocks, and while the Eastern North Pacific (ENP) stock has rebounded, the western stock was feared extirpated. In the post-whaling era, the origin of a small summer aggregation near Sakhalin Island, Russia (which we refer to as the Western North Pacific (WNP) stock) is unclear; this group may include descendants from the original western stock, founders from the eastern stock, or some combination of the two. To clarify the genetic affinities of WNP gray whales, we analyzed whole genome resequencing data for 71 individuals sampled from both geographic regions. Surprisingly, WNP whales are more genetically varied than ENP whales according to principal components and admixture analyses. We present evidence that this structure reflects mixed ancestry in the WNP, where some contemporary whales retain ancestry from the feared-extirpated western population, detectable as “ghost” introgression, while others are of eastern ancestry. Genomic signals based on both single nucleotide polymorphisms and on copy number variants indicate that despite mixed ancestry, the influx of recent eastern gene flow has largely homogenized genomic diversity across the Pacific. These findings highlight the ability of whole-genome data to help resolve questions of extirpation and to clarify complex gene flow dynamics in highly mobile species.