Population structure and connectivity in Indo-Pacific deep-sea mussels of the Bathymodiolus septemdierum complex

Current pressures to mine polymetallic sulfide deposits pose threats to the animal communities found at deep-sea hydrothermal vents. Management plans aimed at preserving these unusual communities require knowledge of historical and contemporary forces that shaped the distributions and connectivity of associated species. As most vent research has focused on the eastern Pacific and mid-Atlantic ridge systems less is known about Indo-Pacific vents, where mineral extraction activities are imminent. Deep-sea mussels (Bivalvia: Mytilidae) of the genus Bathymodiolus include the morphotypic species B. septemdierum, B. brevior, B. marisindicus, and B. elongatus which are among the dominant vent taxa in western Pacific back-arc basins and the Central Indian Ridge. To assess their interpopulational relationships, we examined multilocus genotypes based on DNA sequences from four nuclear and four mitochondrial genes, and allozyme variation encoded by eleven genes. Bayesian assignment methods grouped mussels from seven widespread western Pacific localities into a single cluster, whereas the Indian Ocean mussels were clearly divergent. Thus, we designate two regional metapopulations. Notably, contemporary migration rates among all sites appeared to be low despite limited population differentiation, which highlights the necessity of obtaining realistic data on recovery times and fine-scale population structure to develop and manage conservation units effectively. Future studies using population genomic methods to address these issues in a range of species will help to inform management plans aimed at mitigating potential impacts of deep-sea mining in the Indo-Pacific region

Allopatric and Sympatric Drivers of Speciation in Alviniconcha Hydrothermal Vent Snails

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

Differential patterns of connectivity in Western Pacific hydrothermal vent metapopulations: A comparison of biophysical and genetic models

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 genus Alviniconcha (A. boucheti, A. kojimai, A. strummeri and A. hessleri) that are ecologically dominant taxa at Western Pacific hydrothermal vents. In contrast to predictions from dispersal models, among-basin migration in A. boucheti occurred 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 other Alviniconcha species, suggesting limited between-basin migration for A. kojimai, lack of genetic structure in A. strummeri within the Lau Basin and restricted gene flow between northern and southern A. hessleri populations 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

Axial Seamount

Author Posting. © Oceanography Society, 2010. This article is posted here by permission of Oceanography Society for personal use, not for redistribution. The definitive version was published in Oceanography 23, 1 (2010): 38-39.Axial Seamount is a hotspot volcano superimposed on the Juan de Fuca Ridge (JdFR) in the Northeast Pacific Ocean. Due to its robust magma supply, it rises ~ 800 m above the rest of JdFR and has a large elongate summit caldera with two rift zones that parallel and overlap with adjacent segments of the spreading center

A primer for use of genetic tools in selecting and testing the suitability of set-aside sites protected from deep-sea seafloor massive sulfide mining activities

AbstractSeafloor massive sulfide (SMS) mining will likely occur at hydrothermal systems in the near future. Alongside their mineral wealth, SMS deposits also have considerable biological value. Active SMS deposits host endemic hydrothermal vent communities, whilst inactive deposits support communities of deep water corals and other suspension feeders. Mining activities are expected to remove all large organisms and suitable habitat in the immediate area, making vent endemic organisms particularly at risk from habitat loss and localised extinction. As part of environmental management strategies designed to mitigate the effects of mining, areas of seabed need to be protected to preserve biodiversity that is lost at the mine site and to preserve communities that support connectivity among populations of vent animals in the surrounding region. These “set-aside” areas need to be biologically similar to the mine site and be suitably connected, mostly by transport of larvae, to neighbouring sites to ensure exchange of genetic material among remaining populations. Establishing suitable set-asides can be a formidable task for environmental managers, however the application of genetic approaches can aid set-aside identification, suitability assessment and monitoring. There are many genetic tools available, including analysis of mitochondrial DNA (mtDNA) sequences (e.g. COI or other suitable mtDNA genes) and appropriate nuclear DNA markers (e.g. microsatellites, single nucleotide polymorphisms), environmental DNA (eDNA) techniques and microbial metagenomics. When used in concert with traditional biological survey techniques, these tools can help to identify species, assess the genetic connectivity among populations and assess the diversity of communities. How these techniques can be applied to set-aside decision making is discussed and recommendations are made for the genetic characteristics of set-aside sites. A checklist for environmental regulators forms a guide to aid decision making on the suitability of set-aside design and assessment using genetic tools. This non-technical primer document represents the views of participants in the VentBase 2014 workshop

Species assemblage networks identify regional connectivity pathways among hydrothermal vents in the Northwest Pacific

The distribution of species among spatially isolated habitat patches supports regional biodiversity and stability, so understanding the underlying processes and structure is a key target of conservation. Although multivariate statistics can infer the connectivity processes driving species distribution, such as dispersal and habitat suitability, they rarely explore the structure. Methods from graph theory, applied to distribution data, give insights into both connectivity pathways and processes by intuitively formatting the data as a network of habitat patches. We apply these methods to empirical data from the hydrothermal vent habitats of the Northwest Pacific. Hydrothermal vents are “oases” of biological productivity and endemicity on the seafloor that are imminently threatened by anthropogenic disturbances with unknown consequences to biodiversity. Here, we describe the structure of species assemblage networks at hydrothermal vents, how local and regional parameters affect their structure, and the implications for conservation. Two complementary networks were formed from an extensive species assemblage dataset: a similarity network of vent site nodes linked by weighted edges based on their pairwise assemblage similarity and a bipartite network of species nodes linked to vent site nodes at which they are present. Using these networks, we assessed the role of individual vent sites in maintaining network connectivity and identified biogeographic sub-regions. The three sub-regions and two outlying sites are separated by their spatial arrangement and local environmental filters. Both networks detected vent sites that play a disproportionately important role in regional pathways, while the bipartite network also identified key vent sites maintaining the distinct species assemblages of their sub-regions. These regional connectivity pathways provide insights into historical colonization routes, while sub-regional connectivity pathways are of value when selecting sites for conservation and/or estimating the multivent impacts from proposed deep-sea mining

Phenotypic variation and fitness in a metapopulation of tubeworms (Ridgeia piscesae Jones) at hydrothermal vents

We examine the nature of variation in a hot vent tubeworm, Ridgeia piscesae, to determine how phenotypes are maintained and how reproductive potential is dictated by habitat. This foundation species at northeast Pacific hydrothermal sites occupies a wide habitat range in a highly heterogeneous environment. Where fluids supply high levels of dissolved sulphide for symbionts, the worm grows rapidly in a ‘‘short-fat’’ phenotype characterized by lush gill plumes; when plumes are healthy, sperm package capture is higher. This form can mature within months and has a high fecundity with continuous gamete output and a lifespan of about three years in unstable conditions. Other phenotypes occupy low fluid flux habitats that are more stable and individuals grow very slowly; however, they have low reproductive readiness that is hampered further by small, predator cropped branchiae, thus reducing fertilization and metabolite uptake. Although only the largest worms were measured, only 17% of low flux worms were reproductively competent compared to 91% of high flux worms. A model of reproductive readiness illustrates that tube diameter is a good predictor of reproductive output and that few low flux worms reached critical reproductive size. We postulate that most of the propagules for the vent fields originate from the larger tubeworms that live in small, unstable habitat patches. The large expanses of worms in more stable low flux habitat sustain a small, but long-term, reproductive output. Phenotypic variation is an adaptation that fosters both morphological and physiological responses to differences in chemical milieu and predator pressure. This foundation species forms a metapopulation with variable growth characteristics in a heterogeneous environment where a strategy of phenotypic variation bestows an advantage over specialization

Exploring the ecology of deep-sea hydrothermal vents in a metacommunity framework

© The Author(s), 2018. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Frontiers in Marine Science 5 (2018): 49, doi:10.3389/fmars.2018.00049.Species inhabiting deep-sea hydrothermal vents are strongly influenced by the geological setting, as it provides the chemical-rich fluids supporting the food web, creates the patchwork of seafloor habitat, and generates catastrophic disturbances that can eradicate entire communities. The patches of vent habitat host a network of communities (a metacommunity) connected by dispersal of planktonic larvae. The dynamics of the metacommunity are influenced not only by birth rates, death rates and interactions of populations at the local site, but also by regional influences on dispersal from different sites. The connections to other communities provide a mechanism for dynamics at a local site to affect features of the regional biota. In this paper, we explore the challenges and potential benefits of applying metacommunity theory to vent communities, with a particular focus on effects of disturbance. We synthesize field observations to inform models and identify data gaps that need to be addressed to answer key questions including: (1) what is the influence of the magnitude and rate of disturbance on ecological attributes, such as time to extinction or resilience in a metacommunity; (2) what interactions between local and regional processes control species diversity, and (3) which communities are “hot spots” of key ecological significance. We conclude by assessing our ability to evaluate resilience of vent metacommunities to human disturbance (e.g., deep-sea mining). Although the resilience of a few highly disturbed vent systems in the eastern Pacific has been quantified, these values cannot be generalized to remote locales in the western Pacific or mid Atlantic where disturbance rates are different and information on local controls is missing.LM was supported by NSF OCE 1356738 and DEB 1558904. SB was supported by the NSF DEB 1558904 and the Investment in Science Fund at Woods Hole Oceanographic Institution. MB was supported by the Austrian Science Fund grants P20190-B17 and P16774-B03. LL was supported by NSF OCE 1634172 and the JM Kaplan Fund. MN was supported by NSF DEB 1558904. Y-JW was supported by a Korean Institute of Ocean Science and Technology (KIOST) grant PM60210