Genomics reveals repeated landlocking of diadromous fish on an isolated island

Abstract

Landlocking of diadromous fish in freshwater systems can have significant genomic consequences. For instance, the loss of the migratory life stage can dramatically reduce gene flow across populations, leading to increased genetic structuring, and stronger effects of local adaptation. These genomic consequences have been well-studied in some mainland systems, but the evolutionary impacts of landlocking in island ecosystems are largely unknown. In this study, we used a genotyping-by-sequencing (GBS) approach to examine the evolutionary history of landlocking in common smelt (Retropinna retropinna) on Chatham Island, a small isolated oceanic island 650 km southeast of mainland New Zealand. We examined the relationship among the Chatham Island and mainland smelt, and used coalescent analyses to test the number and timing of landlocking events on Chatham Island. Our genomic analysis, based on 21,135 SNPs across 169 individuals, revealed that the Chatham Island smelt were genomically distinct from the mainland New Zealand fish, consistent with a single ancestral colonisation event of Chatham Island in the Pleistocene. Significant genetic structure was also evident within the Chatham Island smelt, with a diadromous Chatham Island smelt group, along with three geographically structured landlocked groups. Coalescent demographic analysis supported three independent landlocking events, with this loss of diadromy significantly pre-dating human colonisation. Our results illustrate how landlocking of diadromous fish can occur repeatedly across a narrow spatial scale, and highlight a unique system to study the genomic basis of repeated adaptation.