Distance-Limited Larval Replenishment in the Deep-Sea Mussel Gigantidas platifrons Challenges Connectivity-Based Conservation Planning.

Deep-sea chemosynthetic ecosystems, critical for global methane and sulphur cycling, require accurate connectivity data for effective conservation planning amid increasing anthropogenic threats. Because hosts and their environmentally acquired symbionts operate at fundamentally different spatial and temporal scales, we analysed each at the scale appropriate to its biology: host Gigantidas platifrons population structure was assessed both regionally (across 11 Northwest Pacific chemosynthetic sites) and within a single cold seep (Site F, South China Sea) across six shell-length cohorts spanning < 1 year to > 100 years, while the methanotrophic endosymbiont Methyloprofundus sp. was profiled across the same cohorts at Site F to test whether its genetic composition tracks host age or is environmentally homogenized. We found that although the overall host population at Site F is panmictic (ADMIXTURE K = 1; max FST near zero), it exhibits significant fine-scale kinship structure within size cohorts. Kinship decreases sharply with geographic distance (p < 0.001), indicating distance-limited larval replenishment via localized burst recruitment events. In contrast, the methanotrophic symbiont Methyloprofundus sp. is genetically homogeneous across all six host shell-length cohorts at Site F (LD R2 = 0.18879-0.34945; D' = 0.86803-0.91859; max FST = 0.0352; π < 0.0022; overall Tajima's D = -0.5088), consistent with continuous environmental acquisition from a stable, well-mixed local reservoir, thereby buffering the holobiont's core function. Our findings highlight that the host's strong reliance on highly localized recruitment makes population persistence vulnerable to local disturbance. These findings directly challenge conservation models that assume high connectivity and mandate site-specific, holobiont-focused management protecting local breeding stock and age structure.