Dokdo sea lion Zalophus japonicus genome reveals its evolutionary trajectory before extinction

Abstract

Background The Dokdo sea lion (Zalophus japonicus), commonly referred to as Gangchi in Korea also known as the Japanese sea lion, was endemic to the Northwest Pacific coast before becoming extinct in the 1950s. Little is known about its origins and speciation compared to other Otariidae species or how the rapid decline affected the species’ genetic diversity. Results To raise the Dokdo sea lion from this relative obscurity, we sequenced DNA from 16 Z. japonicus’ bone fragments, obtained from Dokdo and Ulleungdo islands in Korea. Our genome-wide SNP-based analyses establish Z. japonicus as the earliest diverged species within its genus, significantly redefining its evolutionary relationship with the California (Z. californianus) and Galapagos (Z. wollebaeki) sea lions. Our research further elucidates the phylogeny of Z. japonicus, shedding light on the complexity of the genetic isolation process within its genus that was prompted by the geographic isolation of the three populations of Zalophus ancestral stock. Conversely, the genetic signature of Dokdo sea lion genome can be modeled as an evolutionary pathway involving gene flow from Otariidae species with shared range. In addition, we discovered, population decline of the Z. japonicus started already over 1,000 years ago, however, Z. japonicus genome maintained a relatively high heterozygosity despite nearing extinction. Conclusions Our genome-scale analysis has eliminated ambiguity in the phylogeny of Z. japonicus and shed light on the evolutionary pathways underlying its speciation and the genetic diversity before its extinction. Broadly, this study highlights the importance of genome-scale analysis for the extinct marine megafauna to elucidate the complexity of their gene flow and subsequent genetic diversities among extant species. Furthermore, this study offers retrospective genomic insights into the extinction process of a carnivorous marine mammal, information that could aid conservation efforts towards extant Otariidae species.