Searching for a Home Port in a Polyvectic World: Molecular Analysis and Global Biogeography of the Marine Worm Polydora hoplura (Annelida: Spionidae)

SIMPLE SUMMARY: Transoceanic shipping and global development of aquaculture are the main vectors for the introduction of marine organisms, as adults or their larvae, to new remote locations. Recent invasions by large species may be well known and documented, while older and smaller-bodied invasions are often hidden and more difficult to detect. In the present study, we investigated, using molecular methods, marine worms that bore into the shells of commercial molluscs on four continents. We have identified them as Polydora hoplura, a species originally described from Italy. The highest genetic diversity was detected in South African population. While high genetic diversity is often regarded as indicative of a species’ natural range, our analysis of the worldwide discovery of P. hoplura calls into question its natural distribution in South Africa. The high genetic diversity of P. hoplura in this region may be the result of a complex dispersal history by ships and aquaculture. We tentatively propose the Northwest Pacific, or at the most the Indo–West Pacific, as its home region, not the Atlantic Ocean or the Eastern Pacific Ocean, and call for further exploration of this hypothesis. ABSTRACT: The spionid polychaete Polydora hoplura Claparède, 1868 is a shell borer widely occurring across the world and considered introduced in many areas. It was originally described in the Gulf of Naples, Italy. Adult diagnostic features are the palps with black bands, prostomium weakly incised anteriorly, caruncle extending to the end of chaetiger 3, short occipital antenna, and heavy sickle-shaped spines in the posterior notopodia. The Bayesian inference analysis of sequence data of four gene fragments (2369 bp in total) of the mitochondrial 16S rDNA, nuclear 18S, 28S rDNA and Histone 3 has shown that worms with these morphological features from the Mediterranean, northern Europe, Brazil, South Africa, Australia, Republic of Korea, Japan and California are genetically identical, form a well-supported clade, and can be considered conspecific. The genetic analysis of a 16S dataset detected 15 haplotypes of this species, 10 of which occur only in South Africa. Despite the high genetic diversity of P. hoplura in South Africa, we tentatively propose the Northwest Pacific, or at the most the Indo–West Pacific, as its home region, not the Atlantic Ocean or the Eastern Pacific Ocean. The history of the discovery of P. hoplura around the world appears to be intimately linked to global shipping commencing in the mid-19th century, followed by the advent of the global movement of commercial shellfish (especially the Pacific oyster Magallana gigas) in the 20th century, interlaced with continued, complex dispersal by vessels and aquaculture. Given that P. hoplura has been detected in only a few of the 17 countries where Pacific oysters have been established, we predict that it may already be present in many more regions. As global connectivity through world trade continues to increase, it is likely that novel populations of P. hoplura will continue to emerge.