Inter-Specific Genetic Exchange Despite Strong Divergence in Deep-Sea Hydrothermal Vent Gastropods of the Genus Alviniconcha

Abstract

Deep hydrothermal vents are highly fragmented and unstable habitats at all temporal and spatial scales. Such environmental dynamics likely play a non-negligible role in speciation. Little is, however, known about the evolutionary processes that drive population-level differentiation and vent species isolation and, more specifically, how geography and habitat specialisation interplay in the species history of divergence. In this study, the species range and divergence of Alviniconcha snails that occupy active Western Pacific vent fields was assessed by using sequence variation data of the mitochondrial Cox1 gene, RNAseq, and ddRAD-seq. Combining morphological description and sequence datasets of the three species across five basins, we confirmed that A. kojimai, A. boucheti, and A. strummeri, while partially overlapping over their range, display high levels of divergence in the three genomic compartments analysed that usually encompass values retrieved for reproductively isolated species with divergences rang from 9% to 12.5% (mtDNA) and from 2% to 3.1% (nuDNA). Moreover, the three species can be distinguished on the basis of their external morphology by observing the distribution of bristles and the shape of the columella. According to this sampling, A. boucheti and A. kojimai form an east-to-west species abundance gradient, whereas A. strummeri is restricted to the Futuna Arc/Lau and North Fiji Basins. Surprisingly, population models with both gene flow and population size heterogeneities among genomes indicated that these three species are still able to exchange genes due to secondary contacts at some localities after a long period of isolation.

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

“…boucheti are largely distributed over the Manus, North Fiji, and Lau Basins, and the Futuna Volcanic Arc, while A . strummeri distribution is limited to the Futuna Arc and the Lau Basin [ 13 , 33 , 34 ]. The Lepetodrilus schrolli species complex is another example of taxa composed of cryptic species in the region [ 17 ], with Lepetodrilus schrolli only found in the Manus Basin while Lepetodrilus aff.…”

“…Contrasted geographic ranges have also been observed for closely related species. For example, amongst the three different species of the snail Alviniconcha found in the South West Pacific, A. kojimai and A. boucheti are largely distributed over the Manus, North Fiji, and Lau Basins, and the Futuna Volcanic Arc, while A. strummeri distribution is limited to the Futuna Arc and the Lau Basin [13,33,34]. The Lepetodrilus schrolli species complex is another example of taxa composed of cryptic species in the region [17], with Lepetodrilus schrolli only found in the Manus Basin while Lepetodrilus aff.…”

Genetic sex determination in three closely related hydrothermal vent gastropods, including one species with intersex individuals

“…The observation that sex is the primary driver of the genetic structure of A. boucheti (Figure 3A) was an unexpected by-product of our analyses of the genetic structure of Alviniconcha gastropods (Castel, 2022;Castel et al, 2022). This was surprising because, given the fragmentation of vent habitats and the disconnected ridge system typical of the Western Pacific back-arc basins (Desbruyères et al, 1994), we expected the geographic distribution of these gastropods (spanning over 4 000-kilometres)…”

“…with known sex, 41 ind. overall), which limits the robustness of the results and may reflect not only a lower abundance but perhaps also a sampling bias linked with the selection of snail patches during collection (a possibility already mentioned in Castel et al, 2022).…”

A step towards measuring connectivity in the deep sea: elemental fingerprints of mollusk larval shells discriminate hydrothermal vent sites

“…Biophysical models suggest that the Eastern regions (North Fiji, Futuna, Lau and Mangatolo) and Manus have no direct connectivity, and that Woodlark acts as a sink region for both ensembles (Matarai et al, 2016). Moreover, recent genetic data on several gastropod species also reported limited migration between the Eastern and Western domains (Castel et al, 2022; Tran Lu Y et al, 2022), and that Woodlark could act as a ‘stepping stone’ in the dispersal of S. tollmanni and other species (Poitrimol et al, 2022). In particular, Tran Lu Y (2022, p. 91) identified a strong genetic break between S. tollmanni populations indicating a complete absence of dispersal between the Manus basin and any site from the Eastern domain, while the two diverging S. tollmanni populations coexist (without admixture) at Woodlark site La Scala.…”