The evolution and population genetics of hydrothermal vent megafauna from the Scotia Sea
Keywords: Peltospiridae
deep-sea biology
hydrothermal vent
Kiwaidae
chemosynthetic ecosystem
Lepetodrilus
East Scotia ridge
Southern Ocean
mid-ocean ridge
biogeography

This project used a variety of genetic markers to investigate the evolution and population genetics of hydrothermal vent fauna that were recovered from the Scotia Sea, in the Atlantic sector of the Southern Ocean.
The origins of one of these species, an undescribed species of Kiwa sp. found on the East Scotia Ridge (ESR) and its constituent family Kiwaidae, a group of vent and seep-associated decapod squat lobsters (infraorder Anomura) was investigated using a concatenated nine-gene dataset and key divergences were dated using fossil calibrations. These results confirm earlier research showing Kiwaidae reside in the superfamily Chirostyloidea, but form a monophyletic clade with the non-chemosynthetic family Chirostylidae and not Eumunididae. Chirostyloid families diverged in the Cretaceous, although extant Kiwaidae radiated in the Eocene, consistent with many other chemosynthetic taxa that appear recently derived. The basal tree position of Pacific species (and the Alaska location of a likely stem-lineage kiwaid fossil) suggests kiwaids originated in the East Pacific. Within a Southern Hemisphere clade, the divergence between the southeastern Pacific K. hirsuta and a non-Pacific lineage (Kiwa sp. ESR and Southwest Indian Ridge kiwaids) is no earlier than 25.9 Ma, consistent with a spread from the Pacific into the Scotia Sea and beyond via now-extinct active ridge connections or mediated by a Miocene onset of the Antarctic Circumpolar Current (ACC) through a newly-opened Drake Passage.
This project also investigated the population genetics of three undescribed species found at two vent fields ~ 440 km apart at either end of the ESR: Kiwa sp., a peltospirid gastropod and Lepetodrilus sp. limpets. Lepetodrilus sp. was also found at the Kemp Caldera, a submerged part of the South Sandwich Islands (SSI). Analyses of cytochrome c oxidase subunit 1 (COI) as well as microsatellite loci developed from Roche 454 sequence libraries revealed no differentiation along the ESR for all three species consistent with panmixia, or the dominance of non-equilibrium processes between vent field colonies within a metapopulation, possibly enhanced further by cold-induced arrested larval development. Despite apparent connectivity along the ESR, both COI and microsatellites revealed differentiation between ESR limpets and Kemp Caldera limpets ~ 95 km to the east, possibly owing to the hydrographic isolation of the caldera. Both COI and microsatellite diversity patterns were consistent with recent (< 1 Ma) demographic expansions for all three species (although the influence of selection sweeps on COI cannot be discounted); a pattern observed worldwide at vent communities and may reflect demographic instability over time as a consequence of the stochastic birth and death of vent colonies within a metapopulation. Different COI bottleneck ages between the three species (excluding the influence of possible selection) as well as the absence of kiwaids and peltospirids at Kemp, have been attributed to differences in life history, in particular larval morphology and presumed dispersal strategy.
These results highlight the role of larval dispersal of vent fauna along active spreading ridges, both in maintaining vent metapopulations across vent colonies prone to stochastic birth and extinction in the short term, but also in the spread of taxa globally and the formation of biogeographic provinces. The likelihood that the three species presented here exist at vents east of the ESR and SSI, prompts further exploration along ridges in the South Atlantic, in order to investigate the effect of the ACC in enhancing gene flow and delineating biogeographic provinces.