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

Abstract

Understanding drivers of biodiversity patterns is essential to evaluate the potential impact of deep-sea mining on ecosystems resilience. While the South West Pacific forms an independent biogeographic province for hydrothermal vent fauna, different degrees of connectivity among basins were previously reported for a variety of species depending on their ability to disperse. In this study, we compared phylogeographic patterns of several vent gastropods across South West Pacific back-arc basins and the newly-discovered La Scala site on the Woodlark Ridge by analysing their genetic divergence using a barcoding approach. We focused on six genera of vent gastropods widely distributed in the region: Lepetodrilus, Symmetromphalus, Lamellomphalus, Shinkailepas, Desbruyeresia and Provanna. A wide-range sampling was conducted at different vent fields across the Futuna Volcanic Arc, the Manus, Woodlark, North Fiji, and Lau Basins, during the CHUBACARC cruise in 2019. The Cox1-based genetic structure of geographic populations was examined for each taxon to delineate putative cryptic species and assess potential barriers or contact zones between basins. Results showed contrasted phylogeographic patterns among species, even between closely related species. While some species are widely distributed across basins (i.e. Shinkailepas tollmanni, Desbruyeresia melanioides and Lamellomphalus) without evidence of strong barriers to gene flow, others are restricted to one (i.e. Shinkailepas tufari complex of cryptic species, Desbruyeresia cancellata and D. costata). Other species showed intermediate patterns of isolation with different lineages separating the Manus Basin from the Lau/North Fiji Basins (i.e. Lepetodrilus schrolli, Provanna and Symmetromphalus spp.). Individuals from the Woodlark Basin were either endemic to this area (though possibly representing intermediate OTUs between the Manus Basin and the other eastern basins populations) or, coming into contact from these basins, highlighting the stepping-stone role of the Woodlark Basin in the dispersal of the South West Pacific vent fauna. Results are discussed according to the dispersal ability of species and the geological history of the South West Pacific.

Coupling large-spatial scale larval dispersal modelling with barcoding to refine the amphi-Atlantic connectivity hypothesis in deep-sea seep mussels

“…Such a scenario may explain how individuals from the same species occur on both sides of the Atlantic and suggest that previously-isolated populations across the Caribbean Sea are currently experiencing a possible secondary contact with the arrival of rare but regular Barbados migrants in the US Atlantic margin waters (see below). Vicariant effects leading to concomitant species divergence at the community scale have also been documented in other deep-sea ecosystems, such as in the backarc-basins of the South West Pacific (Thaler et al, 2011;Thaler et al, 2014;Lee et al, 2019;Poitrimol et al, 2022; or along the East Pacific Rise (Plouviez et al, 2009;Matabos and Jollivet, 2019) in which taxa from several phyla…”

“…harbor a dual symbiosis and relies more on sulfide-derived carbon (Prouty et al, 2016;Van Dover et al, 2003;DeLeo et al, 2022). Contrasted levels of spatial genetic sub-structuring and contemporary gene flow between species that went through the same vicariant effects have also been reported in relation with species-specific life history traits and dispersal abilities in several other oceanic regions (Plouviez et al, 2009;Thaler et al, 2014;Poitrimol et al, 2022;. In the Atlantic Ocean, two sympatric cold-water corals Desmophyllum pertusum and Madrepora oculata showed different post-glacial recolonization histories, most probably as a response to contrasted dispersal abilities and ecological requirements (Boavida et al, 2019).…”

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.…”

The lost vent gastropod species of Lothar A. Beck

“…This has sparked renewed interest in establishing clear and stable descriptions of vent endemic fauna. Superficially similar or plastic morphology across clades makes it difficult to separate species lineages in some vent gastropods (Poitrimol et al 2022). Molecular data for several species in North Fiji and Lau and adjacent regions have shown that the species first recognised as new by Beck are indeed distinct, separate lineages without names (Poitrimol et al 2022;Schwarzpaul 2002).…”

“…Superficially similar or plastic morphology across clades makes it difficult to separate species lineages in some vent gastropods (Poitrimol et al 2022). Molecular data for several species in North Fiji and Lau and adjacent regions have shown that the species first recognised as new by Beck are indeed distinct, separate lineages without names (Poitrimol et al 2022;Schwarzpaul 2002). Since Beck did recognise and describe these species, it is appropriate that his contributions are published and recognised.…”