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 sea snail from Pacific waters that has been a food resource and is commercially important for the coastal fisheries 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, partial sequence of the cytochrome c oxidase subunit I (COI) gene, to compare the obtained results with those from previous microsatellite analyses. 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 2 groups (Groups A and B), with an intermediate haplotype connecting both of the groups. Among eight populations, six were fixed for only one or two haplotypes, and any geographic-genetic correlation was not found; they were probably affected by random drift of the mtDNA lineage. Thus, the results from mtDNA contrasted with those from previous microsatellite analysis, indicating that geographic structure was affected by the restricted gene flow between populations. Our results suggested that N. arthritica diversified 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 long 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 and shows that the output results of such analyses are of great interest for the conservation and management of molluscan species.

Historical shell size reduction of the dogwhelk (Nucella lapillus) across the southern UK

“…Temperature is not the only factor that can affect N. lapillus over time. TBT pollution was a global problem during the 1970’s and 1980’s, occurring in many countries including the UK, Iceland and Japan (Bryan et al 1986 ; Skarphédinsdóttir et al 1996 ; Azuma et al 2015 ; Boyle et al 2016 ). TBT paints leeched into the water from ships and boats, causing the onset of imposex in female dogwhelks across the southern UK coast, especially in areas of heavy boat and ship traffic (Bryan et al 1986 ; Spence et al 1990 ).…”

Systematics and Distributions of Upper Bathyal Species in Bathyancistrolepis, a Deep-Sea Whelk Genus Endemic to the Northwest Pacific (Gastropoda: Buccinidae)

“…They occur on all types of seafloor, ranging from intertidal rocky shores to hadal trenches (Kantor et al, 2020(Kantor et al, , 2022. Buccinids are particularly abundant and diverse in the shelf and bathyal depth zones of the Northwest Pacific (Kosyan and Kantor, 2009), where they are widely harvested for food (e.g., Fujinaga et al, 2006;Yamakami and Wada, 2021) and have served as suitable model organisms for studying the biogeography of deep-sea benthos (e.g., Amano, 2004;Iguchi et al, 2007;Azuma et al, 2015). The latest molecular phylogeny of the superfamily Buccinoidea (Kantor et al, 2022) has provided the basis for the current classification of the family, encompassing eight subfamilies and 34 extant genera (MolluscaBase, 2023).…”