Origin, diversity, and biogeography of Antarctic scale worms (Polychaeta: Polynoidae): a wide-scale barcoding approach

Aim: The Antarctic marine environment hosts diversified and highly endemic benthos owing to its unique geologic and climatic history. Current warming trends have increased the urgency of understanding Antarctic species history to predict how environmental changes will impact ecosystem functioning. Antarctic benthic lineages have traditionally been examined under three hypotheses: 1) high endemism and local radiation, 2) emergence of deep-sea taxa through thermohaline circulation, 3) species migrations across the Polar Front. In this study, we investigated which hypotheses best describe benthic invertebrate origins by examining Antarctic scale worms.

Location: Southern Ocean, Kerguelen archipelago, South American peninsula, Indian Ocean, New Zealand.

Taxon: Scale worm polychaetes (Polynoidae).

Methods: We amassed 670 polynoids from the Southern Ocean and neighbouring areas and performed phylogenetic reconstructions to identify lineages across geographic regions, aided by mitochondrial markers Cytochrome c oxidase subunit I (Cox1) and 16S ribosomal RNA (16S). Additionally, we produced haplotype networks at the species scale to examine genetic diversity, biogeographic separations, and past demography.

Results: The Cox1 dataset provided the most illuminating insights into the evolution of polynoids. Eunoe sp. was present at South America and Kerguelen, in favour of the latter acting as a migration crossroads. Harmothoe fuligineum, widespread around the Antarctic continent, was also present but isolated at Kerguelen, possibly resulting from historical freeze-thaw cycles. The genus Polyeunoa appears to have diversified prior to colonizing the continent, leading to the cooccurrence of at least three cryptic species around the Southern and Indian Oceans. Analyses identified that nearly all populations are presently expanding following a bottleneck event, possibly caused by habitat reduction from the last glacial episodes.

Main Conclusions: This study details the largest phylogenetic dataset assembled to date for Antarctic polynoids. These findings provide insight into past demographic events experienced by Antarctic marine benthos and identify multiple origin scenarios for contemporary polynoids.