Molecular phylogenetic re-evaluation of deep-sea holothuroid genus Pannychia based on COI gene and genome-wide SNPs data

The deep-sea has traditionally been believed an “open” environment with few barriers to gene flow, and many species are assumed to have wide distributions. Many sea cucumber species, known as major megabenthos in the deep-sea ecosystem, were also thought to have a worldwide distribution based on morphological identifications. Pannychia is one of the common holothuroid genera at the bathyal seafloor in the Pacific Ocean, whose taxonomy was revised to six valid species in the last decade. However, the actual species diversity of Pannychia is still unclear and requires global revision. Here we propose a revision of Pannychia based on the combined results of morphological characteristics and two different kinds of molecular phylogenetic methods, DNA barcoding of the partial cytochrome c oxidase subunit I (COI) gene and a genome-wide single-nucleotide polymorphisms (SNPs). We examined 178 individuals of Pannychia collected from the North and South Pacific, Indian and Southern waters from 1986 to 2019. Phylogenetic analyses based on COI and SNPs datasets detected the same ten distinct clades within Pannychia. We conclude here that these clades should be treated as separate species, including one species, P. fecundum comb. nov., which we have raised from a synonymy with P. moseleyi. We suggest that P. moseleyi has been misidentified as a species, with the species diversity of Pannychia underestimated due to partly overlapping distributions of species with similar morphology leading to biological species boundaries being overlooked. We demonstrate the effectiveness of using whole-genome SNPs data in revising species diversity and taxonomy in deep-sea widely distributed species.