Phylogeography of Neptune whelk (Neptunea arthritica) suggests sex-biased impact of tributyltin pollution and overfishing around northern Japan

Abstract

The Neptune whelk, Neptunea arthritica, is a sublittoral snail from Pacific waters that is a food resource and supports a commercially important fishery in northern Japan. This species showed a severe decline during the 1970s and 1980s, possibly because of overfishing, imposex caused by tributyltin (TBT) pollution and parasite infection. In the present study, we investigated genetic variation among the populations of N. arthritica from eight localities in northern Japan, including Hokkaido and Aomori, using a mitochondrial DNA (mtDNA) marker, a partial sequence of the cytochrome c oxidase subunit I (COI) gene. We also addressed the evolutionary history of N. arthritica and human impact on the population genetic profiles of this species. The parsimony network showed 14 COI haplotypes separated into two groups (Groups A and B), with an intermediate haplotype connecting both groups. Among eight populations, six were fixed for only one or two haplotypes, and no geographic-genetic correlation was found; they were probably affected by random drift. These results contrasted with those from previous microsatellite analysis, which indicated that geographic structure was the result of restricted gene flow between populations. Our results suggested that N. arthritica diverged into Groups A and B during the Pliocene; however, recent TBT pollution and size-selective fishing pressure have reduced genetic diversity and concealed the natural population structure. The present study also suggested that human impact may cause longstanding and possibly irreversible modification of ecosystems, particularly for species forming discrete and relatively small local populations, such as N. arthritica. Thus, the combined use of mtDNA and microsatellite genetic data provides a powerful tool to investigate the health of biodiversity in molluscs.