Description: Highlights: • Mid-Atlantic vent mussel populations are contemporarily isolated • Population connectivity can only be maintained in a stepwise manner • Four mussel lineages exist on the Mid-Atlantic Ridge • Recolonization of perturbed vent localities is uncertain Summary: Deep-sea hydrothermal vents are patchily distributed ecosystems inhabited by specialized animal populations that are textbook meta-populations. Many vent-associated species have free-swimming, dispersive larvae that can establish connections between remote populations. However, connectivity patterns among hydrothermal vents are still poorly understood because the deep sea is undersampled, the molecular tools used to date are of limited resolution, and larval dispersal is difficult to measure directly. A better knowledge of connectivity is urgently needed to develop sound environmental management plans for deep-sea mining. Here, we investigated larval dispersal and contemporary connectivity of ecologically important vent mussels (Bathymodiolus spp.) from the Mid-Atlantic Ridge by using high-resolution ocean modeling and population genetic methods. Even when assuming a long pelagic larval duration, our physical model of larval drift suggested that arrival at localities more than 150 km from the source site is unlikely and that dispersal between populations requires intermediate habitats (“phantom” stepping stones). Dispersal patterns showed strong spatiotemporal variability, making predictions of population connectivity challenging. The assumption that mussel populations are only connected via additional stepping stones was supported by contemporary migration rates based on neutral genetic markers. Analyses of population structure confirmed the presence of two southern and two hybridizing northern mussel lineages that exhibited a substantial, though incomplete, genetic differentiation. Our study provides insights into how vent animals can disperse between widely separated vent habitats and shows that recolonization of perturbed vent sites will be subject to chance events, unless connectivity is explicitly considered in the selection of conservation areas.

Description: In highly fragmented and relatively stable cold-seep ecosystems, species are expected to exhibit high migration rates and long-distance dispersal of long-lived pelagic larvae to maintain genetic integrity over their range. Accordingly, several species inhabiting cold seeps are widely distributed across the whole Atlantic Ocean, with low genetic divergence between metapopulations on both sides of the Atlantic Equatorial Belt (AEB, i.e. Barbados and African/European margins). Two hypotheses may explain such patterns: (i) the occurrence of present-day gene flow or (ii) incomplete lineage sorting due to large population sizes and low mutation rates. Here, we evaluated the first hypothesis using the cold seep mussels Gigantidas childressi, G. mauritanicus, Bathymodiolus heckerae and B. boomerang. We combined COI barcoding of 763 individuals with VIKING20X larval dispersal modelling at a large spatial scale not previously investigated. Population genetics supported the parallel evolution of Gigantidas and Bathymodiolus genera in the Atlantic Ocean and the occurrence of a 1-3 Million-year-old vicariance effect that isolated populations across the Caribbean Sea. Both population genetics and larval dispersal modelling suggested that contemporary gene flow and larval exchanges are possible across the AEB and the Caribbean Sea, although probably rare. When occurring, larval flow was eastward (AEB - only for B. boomerang) or northward (Caribbean Sea - only for G. mauritanicus). Caution is nevertheless required since we focused on only one mitochondrial gene, which may underestimate gene flow if a genetic barrier exists. Non-negligible genetic differentiation occurred between Barbados and African populations, so we could not discount the incomplete lineage sorting hypothesis. Larval dispersal modelling simulations supported the genetic findings along the American coast with high amounts of larval flow between the Gulf of Mexico (GoM) and the US Atlantic Margin, although the Blake Ridge population of B. heckerae appeared genetically differentiated. Overall, our results suggest that additional studies using nuclear genetic markers and population genomics approaches are needed to clarify the evolutionary history of the Atlantic bathymodioline mussels and to distinguish between ongoing and past processes.

Description: Ocean ecosystems are at the forefront of the climate and biodiversity crises, yet we lack a unified approach to assess their state and inform sustainable policies. This blueprint is designed around research capabilities and cross-sectoral partnerships. We highlight priorities including integrating basin-scale observation, modelling and genomic approaches to understand Atlantic oceanography and ecosystem connectivity; improving ecosystem mapping; identifying potential tipping points in deep and open ocean ecosystems; understanding compound impacts of multiple stressors including warming, acidification and deoxygenation; enhancing spatial and temporal management and protection. We argue that these goals are best achieved through partnerships with policy-makers and community stakeholders, and promoting research groups from the South Atlantic through investment and engagement. Given the high costs of such research (€800k to €1.7M per expedition and €30–40M for a basin-scale programme), international cooperation and funding are integral to supporting science-led policies to conserve ocean ecosystems that transcend jurisdictional borders.