Scaly-foot snails from eight hydrothermal vents map invisible “highways” and “roadblocks” in the deep sea
—Population genomic analyses reconstruct dispersal over time and identify priority areas for conservation—

1. Key Points

• Deep-sea hydrothermal vents are like “islands” scattered across the seafloor for vent-endemic species that can live nowhere else. The overall picture of how these species disperse and connect among vent fields separated by hundreds of kilometres has remained unclear—especially in the Indian Ocean, where surveys are limited.
• Focusing on the iconic vent-endemic scaly-foot snail (Chrysomallon squamiferum), we conducted population genomic analyses to reconstruct the dispersal history across eight Indian Ocean vent fields. Present-day populations form five major genetic groups; notably, the southernmost Longqi-Duanqiao vent fields and the northernmost Wocan vent field show very high genetic distinctiveness. Such populations are strong candidates for being prioritized in conservation planning in the light of upcoming deep-sea mining.
• By integrating reconstructions of contemporary and historical gene flow with physical ocean model simulations, we found that dispersal is predominantly south-to-north overall, while large transform faults on the seafloor act as dispersal barriers that hinder larval exchange. We also show that “ghost populations”, extinct vent fields or as-yet-undiscovered sites, likely played a major role in shaping today’s genetic diversity.

An international collaborative research team including Dr. Chong Chen and Dr. Ken Takai at the Institute for Extra-cutting-edge Science and Technology Avant-garde Research (X-star), Japan Agency for Marine-Earth Science and Technology (JAMSTEC; President: Hiroyuki Yamato) has reconstructed fine-scale genetic connectivity across deep-sea hydrothermal vents in the Indian Ocean and through time by combining genomic methods and particle-tracing ocean current simulations, using the iconic ironclad scaly-foot snail (Chrysomallon squamiferum) as a model species.

The scaly-foot snail is an endemic species of the Indian Ocean vents and is famous for carrying hard, imbricating scales on its foot that are often infused with iron sulfide. It is also known for its one-of-a-kind survival strategy: it relies on chemosynthetic bacteria inside cells of its esophageal gland for energy, and detoxifies sulfide by excreting sulfur metabolites into its scales. Two well-known populations are the so-called “black” scaly-foot from Kairei field whose scales are infused with iron sulfide, and the “white” scaly-foot from Solitaire field whose scales lack iron. In recent years, a succession of new vent fields has been discovered in the Indian Ocean, and scaly-foot snails have now been collected from at least eight vent fields across three mid-ocean ridges (Figure 1).

Deep-sea hydrothermal vents host chemosynthetic ecosystems formed by unique endemic species such as the scaly-foot snail. At the same time, hydrothermal massive sulfide deposits at vents are considered potential targets for future mineral resource development. In the Indian Ocean, most vent fields lie in areas beyond national jurisdiction (the high seas) and fall within exploration contract areas approved by the International Seabed Authority (ISA) for Germany, India, South Korea, and China. There is an urgent need to compile information for science-based conservation and environmental impact assessment, yet surveys and research on vent endemics remain insufficient. In particular, fine-scale patterns of genetic connectivity among vent fields is essential for evaluating conservation priority of each vent field but has remained unclear in the Indian Ocean.

Our study is the first to undertake population-scale genome analysis of a vent-endemic species in the Indian Ocean. Using a genome-wide dataset of 14,309,443 high-confidence single nucleotide polymorphisms (SNPs), we found that the present-day scaly-foot snails are divided into five genetic groups (Figure 2). Furthermore, the reconstruction of historical demographics (Figure 3) showed that the scaly-foot snail dispersed northward from near the Longqi field on the Southwest Indian Ridge over a span of approximately 200,000~400,000 years to reach the Wocan field on the Carlsberg Ridge, the northernmost known locality. Among the five genetic groups, the Longqi and Wocan fields show particularly high genetic distinctiveness, highlighting them as high-priority candidates for conservation planning.

Combining with physical ocean model simulations with tracer particles functioning as hypothetical scaly-foot snail larvae (Figure 4), we find that the dispersal of the scaly-foot snail appears to have been shaped by deep currents flowing northward from the Southern Ocean, dispersal barriers created by transform faults that offset ridge axes, and “ghost populations” that were either never discovered or were once active but are now inactive. We hypothesized that a known vent plume signal that has not been confirmed by submersible dive on the Southwest Indian Ridge (SWIR Plume, Figure 4) and an extinct, inactive vent field known from the northern Central Indian Ridge (CIR Extinct, Figure 4) are likely candidates for such “ghost populations”, and confirmed their ability to connect nearby populations using physical ocean model simulations.

Since many marine organisms disperse through larval dispersal, the importance of transform faults as dispersal barriers and the results of particle-tracer simulations shown here may apply not only to other vent-endemic species with dispersal capacities similar to the scaly-foot snail, but also to other deep-sea ecosystems such as seamounts on mid-ocean ridges. Our results further suggest that connectivity breaks caused by transform faults may have contributed to the formation of deep-sea biogeographic provinces at a global scale.

The findings of this study are grounded in extensive foundational ocean observations, including multi-site biological sampling required for population genomics, physical oceanographic surveys to characterise seawater circulation, and geophysical surveys to map seafloor topography. By continuing ocean expeditions and advanced research based on those observations, we will provide essential baseline knowledge for environmental impact assessment of deep-sea environments including hydrothermal vents, and ultimately contribute to the formulation of conservation plans for the deep seafloor.

This work is will be published in Current Biology on February 12 (Japan Standard Time).

Figure 1. Geographic distribution of the eight hydrothermal vent fields inhabited by the scaly-foot snail, and representative photographs of individuals from each site. The eight vent fields are located on the Southwest Indian Ridge (SWIR), Central Indian Ridge (CIR), and Carlsberg Ridge (CR).

Figure 2. Population analyses of scaly-foot snails from the eight vent fields. (A) Pairwise F_ST values among vent-field combinations of scaly-foot snails. F_ST ranges from 0 to 1, and values closer to 1 indicate greater genetic differentiation. (B) Principal component analysis (PCA) showing genetic differences among populations. The results indicate low differentiation within the pairs Longqi-Duanqiao, Solitaire-Kairei, and Onnuri-Onnare; these pairs were therefore combined as single genetic groups (dashed circles). (C) Population structure and genetic components of each individual inferred by the software ADMIXTURE, shown for K = 3-5 assumed genetic groups.

Figure 3. Demographic model of scaly-foot snail populations through time (built using population parameters estimated with the software fastsimcoal2). Arrows indicate the direction of gene flow; dashed arrows represent ancestral (historical) gene flow and solid arrows represent gene flow among extant populations. Arrow thickness and values indicate gene-flow intensity (migration rate per year). Ghost populations (G0-G3) inferred from genetic analyses are shown in grey. The vertical axis indicates time before present (values in parentheses indicate 95% confidence intervals).

Figure 4. Physical ocean model simulation with particle-tracking that mimic larval dispersal driven by ocean currents. Particles representing scaly-foot snail larvae were released from each vent field and from two candidate ghost-population sites (an unconfirmed vent field and an inactive vent field), and their transport by deep currents was simulated. (A) Particle distributions after 1, 6, and 12 years. Colour intensity indicates (log-transformed) particle density. (B) The relative amount of particles transported from each source site (shown along the bottom) to each sink or receiving site (shown on the left) over a span of 15 years. Colour intensity indicates (log-transformed) particle density. The horizontal axis represents time (years) and the vertical axis represents depth (km).