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

Abstract

Hydrothermal vents form archipelagos of ephemeral deep‐sea habitats that raise interesting questions about the evolution and dynamics of the associated endemic fauna, constantly subject to extinction‐recolonization processes. These metal‐rich environments are coveted for the mineral resources they harbour, thus raising recent conservation concerns. The evolutionary fate and demographic resilience of hydrothermal species strongly depend on the degree of connectivity among and within their fragmented metapopulations. In the deep sea, however, assessing connectivity is difficult and usually requires indirect genetic approaches. Improved detection of fine‐scale genetic connectivity is now possible based on genome‐wide screening for genetic differentiation. Here, we explored population connectivity in the hydrothermal vent snail Ifremeria nautilei across its species range encompassing five distinct back‐arc basins in the Southwest Pacific. The global analysis, based on 10,570 single nucleotide polymorphism (SNP) markers derived from double digest restriction‐site associated DNA sequencing (ddRAD‐seq), depicted two semi‐isolated and homogeneous genetic clusters. Demogenetic modeling suggests that these two groups began to diverge about 70,000 generations ago, but continue to exhibit weak and slightly asymmetrical gene flow. Furthermore, a careful analysis of outlier loci showed subtle limitations to connectivity between neighbouring basins within both groups. This finding indicates that migration is not strong enough to totally counterbalance drift or local selection, hence questioning the potential for demographic resilience at this latter geographical scale. These results illustrate the potential of large genomic data sets to understand fine‐scale connectivity patterns in hydrothermal vents and the deep sea.

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

“…In addition, levels of divergence were not correlated with geographic distances. A geographic split between populations of the Manus Basin and the North Fiji/Lau Basins was already reported for a number of taxa, including Ifremeria nautilei (a large symbiotic gastropod), the shrimp Rimicaris variabilis , the crab Austinograea alayseae and the limpet Lepetodrilus schrolli [ 19 , 30 – 32 , 71 ]. This study is however the first to publish genetic data associated with the Woodlark Basin and its stepping-stone role on the vent fauna dissemination.…”

“…Connection is predicted to be successful westward from the Woodlark Basin to the Manus Basin, and from the Lau to the North Fiji Basins, once every ~5 000 to ~12 000 years considering a pelagic larval duration of 82 days between 100 to 1 500 m [ 28 ]. However, eastward gene flow from the Manus Basin to the North Fiji and Lau Basins has been suggested for several taxa [ 19 , 26 , 30 , 31 ] but not Ifremeria nautilei when looking at more contemporary gene flow [ 71 ]. Different larval behaviours have already been observed between North West Pacific Shinkailepas species [ 52 , 86 ].…”

Landscape genomics of the American lobster (Homarus americanus)

“…So far, while neutral genetic markers have been considered essential to properly document population structure (Landguth & Balkenhol, 2012 ; Luikart et al, 2003 ), another important consideration pertains to the interpretation of “outlier loci” for delineating populations (reviewed in Bernatchez, 2016 ). Although it has been common practice to discard such markers when inferring population genetic structure and connectivity, some have argued in favour of retaining such markers, especially when studying weakly differentiated systems such as those involving marine (Attard et al, 2018 ; Gagnaire et al, 2015 ; Milano et al, 2014 ; Tran Lu Y et al, 2022 ) or terrestrial organisms, such as many plant species (Keller et al, 2018 ; Tyrmi et al, 2020 ) but also a number of terrestrial animal species (Batista et al, 2016 ). Indeed, genomic regions under divergent selection (including adjacent genomic regions in linkage disequilibrium [LD] with the targets of selection) are often characterized by stronger restriction of gene flow among populations (locally affecting N e and m ) compared to the genome‐wide background, which can promote evolution of reproductive isolation (Barton & Bengtsson, 1986 ).…”

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.…”

“…, McVeigh et al 2017). Another class of methods use population genetics to infer migration between populations (Baco et al 2016; Breusing et al 2016; Tran Lu Y et al, 2022). Genetic methods, however, are limited in many marine invertebrates because large populations experience weak genetic drift and therefore weak genetic structure regardless of migration rates (Gagnaire et al, 2015).…”