Population connectivity of the hydrothermal-vent limpet Shinkailepas tollmanni in the Southwest Pacific (Gastropoda: Neritimorpha: Phenacolepadidae)

Abstract

The Southwest Pacific represents an independent biogeographic province for deep-sea hydrothermal vent fauna. Different degrees of genetic connectivity among vent fields in Manus, North Fiji and Lau Basins have been reported for various molluscan and crustacean species, presumably reflecting their different levels of dispersal ability as swimming larvae. The present study investigates the population connectivity of the hydrothermal vent limpet Shinkailepas tollmanni (family Phenacolepadidae) in the Southwest Pacific. Our analyses using mitochondrial COI-gene sequences and shell morphometric traits suggest a panmictic population structure throughout its geographic and bathymetric ranges, spanning 4,000 km from the westernmost Manus Basin (151ºE; 1,300 m deep) to the easternmost Lau Basin (176ºE; 2,720 m). The measurements of its embryonic and larval shells demonstrate that the species hatches as a planktotrophic veliger larva with an embryonic shell diameter of 170-180 μm and settles at the vent environment with the larval shell diameter of 750-770 μm. This substantial growth as a feeding larva, ca. 80 times in volume, is comparable or even greater than those of confamilial species in the hydrothermal-vent and methane-seep environments in the Northwest Pacific and Atlantic Oceans. Large pigmented eyes in newly settled juveniles are another common feature in this and other phenacolepadids inhabiting the chemosynthetic environments. These results put together suggest that the larvae of S. tollmanni migrate vertically from deep-sea vents to surface waters to take advantages of richer food supplies and faster currents and stay pelagic for an extended period of time (> 1 year), as previously indicated for the confamilial species.

Contrasted phylogeographic patterns of hydrothermal vent gastropods along South West Pacific: Woodlark Basin, a possible contact zone and/or stepping-stone

“…tollmanni specimens from all basins and the Futuna Volcanic Arc belong to a single phylogenetic lineage which also comprises the S . tollmanni sequences from Yahagi et al [ 29 ] and Fukumori et al [ 50 ] (Figs 3 and 6 ). The analysis of the 75 S .…”

“…In addition, some larvae like those of the vent polychaete Alvinella pompejana may arrest their development in cold water until suitable conditions are encountered [ 84 , 85 ], resulting in long-lasting propagules. Shinkailepas and Desbruyeresia larvae have been shown to be planktotrophic [ 29 , 40 , 42 , 52 ] but most of their congeneric species exhibit highly fragmented genetic structure and species diversification. Variable larval lifespan and/or ontogenic behaviour could explain the contrasted distributions within these genera, as connectivity between basins would vary according to PLD and depth of dispersal [ 28 ].…”

“…While for some species larvae are believed to migrate to the surface, thus taking advantage of food resources and stronger currents, others remain close to the seabed, inducing different dispersal capacities. Vertical migration to shallow water has been suggested for Shinkailepas tollmanni for which larvae, although encapsulated until they reach their trochophore stage, are thought to stay pelagic for over a year [ 29 ], potentially allowing long-distance dispersal through the Manus, Woodlark, North Fiji, and Lau Basins, and the Futuna Volcanic Arc. Conversely, in the specific case of Shinkailepas tufari , larvae might be more likely to stay near the seabed which could account for their more limited distribution ranges.…”

“…Genetic studies on several gastropods and crustaceans based on cytochrome oxidase I gene ( Cox1 ) and/or microsatellite loci confirmed the occurrence of variable phylogeographic patterns from large scale connectivity with only one panmictic population [ 29 ] to strong regional genetic differences that separates the Manus Basin populations from those of the North Fiji and Lau Basins [ 30 – 32 ]. Contrasted geographic ranges have also been observed for closely related species.…”

Subtle limits to connectivity revealed by outlier loci within two divergent metapopulations of the deep‐sea hydrothermal gastropod Ifremeria nautilei

“…Moreover, this latter species is characterized by additional intrabasin structuring. In contrast, the limpet Shinkailepas tollmani does not show any differentiation at any of these scales (Yahagi et al, 2020). However, due to the use of only a limited number of markers, none of these studies have reached the resolution necessary for the fine‐scale assessment of connectivity in these species.…”