Disentangling invasions in the sea: molecular analysis of a global polychaete species complex (Annelida: Spionidae: Pseudopolydora paucibranchiata)

The spionid polychaete Pseudopolydora paucibranchiata (Okuda, 1937) was originally described from Japan and has since been reported as a non-indigenous species in soft bottom communities in the Northeast Pacific, the Mediterranean Sea, around Europe, Australia, Brazil, and Florida. The diagnostic features of the adults are palps with ramified yellow chromatophores, prostomium rounded anteriorly, short occipital antenna on the caruncle, and a small disc-like pygidium. We collected Pseudopolydora with these features from locations worldwide and compared them by a molecular analysis. The Bayesian analysis of the combined dataset of three genetic markers (mitochondrial 16S rDNA, nuclear 28S rDNA and Histone 3; 811 bp in total) showed that the worms form a monophyletic group comprising four genetically different clades. We name this group the P. paucibranchiata complex and consider the clades as four pseudocryptic species. The largest examined clade comprises individuals from the Pacific Canada (British Columbia), Russia (Sea of Japan), South Korea (East Sea), Italy (Tyrrhenian and Ionian Seas), Australia (Victoria), Netherlands, and Japan, which we identify as P.paucibranchiata. The morphology, reproductive biology and ecology of P. paucibranchiata are briefly reviewed. The other three clades are referred to as Pseudopolydora vexillosa Radashevsky and Hsieh, 2000 (Vietnam, Nha Trang Bay), Pseudopolydora sp. A (Australia, Northern Territory), and Pseudopolydora sp. B (Kuwait, Arabian Gulf). We explain the occurrence of P. paucibranchiata outside of the Northwest Pacific by unintentional human-mediated transportation in ballast water and/or with commercial oyster movements in aquaculture operations, followed by successful invasions. Keywords Polychaetes Biological invasions Distribution Cryptic species Molecular systematics Introduction The spionid polychaete worm Pseudopolydora paucibranchiata (Okuda, 1937) is native to the Northwest Pacific Ocean, including Japan (its type locality, in Hiroshima Prefecture) and along the mainland coast of the Sea of Japan (East Sea), East China Sea and the Yellow Sea in Russia, Korea and northern China (Imajima and Hartman 1964; Paik 1989; Radashevsky 1993; Sun 1994; Sato-Okoshi 2000; Zhou et al. 2010). Beginning in the 1950s, however, reports of P. paucibranchiata began appearing on the well-explored Pacific coast of North America, by the 1970s it was reported from Australia and New Zealand, and by the 1980s–1990s from European localities. Over the past half-century, many workers attributed these extralimital records to human-mediated introductions, through a variety of vectors (Carlton 2001; Minchin and Gollasch 2002, and below). All of these records outside of the Northwest Pacific were based on morphological identifications. Molecular characterization of P. paucibranchiata had been previously reported only for Japanese populations (Abe et al. 2016). Adults of P. paucibranchiata build silty tubes and often form dense populations in soft sediments in shallow waters. They have been characterized morphologically by having palps with ramified yellow chromatophores, prostomium rounded anteriorly, short occipital antenna on the caruncle, and a small disc-like pygidium without dorso-lateral extensions (Okuda 1937; Imajima and Hartman 1964; Radashevsky 1993). We collected Pseudopolydora worms with these characteristics during taxonomic and other surveys worldwide. The purpose of the present study was to compare these worms by molecular analyses to clarify their relationships.