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Hydrothermal ecosystems face threats from planned deep‐seabed mining activities, despite the fact that patterns of realized connectivity among vent‐associated populations and communities are still poorly understood. Since populations of vent endemic species depend on larval dispersal to maintain connectivity and resilience to habitat changes, effective conservation strategies for hydrothermal ecosystems should include assessments of metapopulation dynamics. In this study, we combined population genetic methods with biophysical models to assess strength and direction of gene flow within four species of the genusAlviniconcha(A. boucheti,A. kojimai,A. strummeriandA. hessleri) that are ecologically dominant taxa at Western Pacific hydrothermal vents. In contrast to predictions from dispersal models, among‐basin migration inA. bouchetioccurred predominantly in an eastward direction, while populations within the North Fiji Basin were clearly structured despite the absence of oceanographic barriers. Dispersal models and genetic data were largely in agreement for the otherAlviniconchaspecies, suggesting limited between‐basin migration forA. kojimai, lack of genetic structure inA. strummeriwithin the Lau Basin and restricted gene flow between northern and southernA. hessleripopulations in the Mariana back‐arc as a result of oceanic current conditions. Our findings show that gene flow patterns in ecologically similar congeneric species can be remarkably different and surprisingly limited depending on environmental and evolutionary contexts. These results are relevant to regional conservation planning and to considerations of similar integrated analyses for any vent metapopulations under threat from seabed mining.

 

Symbioses between invertebrate animals and chemosynthetic bacteria form the basis of hydrothermal vent ecosystems worldwide. In the Lau Basin, deep-sea vent snails of the genus Alviniconcha associate with either Gammaproteobacteria (A. kojimai, A. strummeri) or Campylobacteria (A. boucheti) that use sulfide and/or hydrogen as energy sources. While the A. boucheti host–symbiont combination (holobiont) dominates at vents with higher concentrations of sulfide and hydrogen, the A. kojimai and A. strummeri holobionts are more abundant at sites with lower concentrations of these reductants. We posit that adaptive differences in symbiont physiology and gene regulation might influence the observed niche partitioning between host taxa. To test this hypothesis, we used high-pressure respirometers to measure symbiont metabolic rates and examine changes in gene expression among holobionts exposed to in situ concentrations of hydrogen (H2: ~25 µM) or hydrogen sulfide (H2S: ~120 µM). The campylobacterial symbiont exhibited the lowest rate of H2S oxidation but the highest rate of H2 oxidation, with fewer transcriptional changes and less carbon fixation relative to the gammaproteobacterial symbionts under each experimental condition. These data reveal potential physiological adaptations among symbiont types, which may account for the observed net differences in metabolic activity and contribute to the observed niche segregation among holobionts.

 

Symbiont specificity, both at the phylotype and strain level, can have profound consequences for host ecology and evolution. However, except for insights from a few model symbiosis systems, the degree of partner fidelity and the influence of host versus environmental factors on symbiont composition are still poorly understood. Nutritional symbioses between invertebrate animals and chemosynthetic bacteria at deep-sea hydrothermal vents are examples of relatively selective associations, where hosts affiliate only with particular, environmentally acquired phylotypes of gammaproteobacterial or campylobacterial symbionts. In hydrothermal vent snails of the sister genera Alviniconcha and Ifremeria , this phylotype specificity has been shown to play a role in habitat distribution and partitioning among different holobiont species. However, it is currently unknown if fidelity goes beyond species-level associations and influences genetic structuring, connectivity, and habitat adaptation of holobiont populations. We used metagenomic analyses to assess sequence variation in hosts and symbionts and identify correlations with geographic and environmental factors. Our analyses indicate that host populations are not differentiated across an ∼800-km gradient, while symbiont populations are clearly structured between vent locations due to a combination of neutral and selective processes. Overall, these results suggest that host individuals flexibly associate with locally adapted strains of their specific symbiont phylotypes, which supports a long-standing but untested paradigm of the benefits of horizontal transmission. Symbiont strain flexibility in these snails likely enables host populations to exploit a range of habitat conditions, which might favor widespread genetic connectivity and ecological resilience unless physical dispersal barriers are present. 

Abstract Despite significant advances in our understanding of speciation in the marine environment, the mechanisms underlying evolutionary diversification in deep-sea habitats remain poorly investigated. Here, we used multigene molecular clocks and population genetic inferences to examine processes that led to the emergence of the six extant lineages of Alviniconcha snails, a key taxon inhabiting deep-sea hydrothermal vents in the Indo-Pacific Ocean. We show that both allopatric divergence through historical vicariance and ecological isolation due to niche segregation contributed to speciation in this genus. The split between the two major Alviniconcha clades (separating A. boucheti and A. marisindica from A. kojimai, A. hessleri, and A. strummeri) probably resulted from tectonic processes leading to geographic separation, whereas the splits between co-occurring species might have been influenced by ecological factors, such as the availability of specific chemosynthetic symbionts. Phylogenetic origin of the sixth species, Alviniconcha adamantis, remains uncertain, although its sister position to other extant Alviniconcha lineages indicates a possible ancestral relationship. This study lays a foundation for future genomic studies aimed at deciphering the roles of local adaptation, reproductive biology, and host–symbiont compatibility in speciation of these vent-restricted snails.