Abstract: 

Deep-sea hydrothermal vents and hydrocarbon seeps are two types of extreme habitats often patchily distributed along oceanic spreading centers and tectonically active continental margins. Recent investigations have shown that certain species are capable of inhabiting both habitat types. The co-occurrence raises fundamental evolutionary questions regarding how these macrobenthos achieve population connectivity across spatially fragmented and geochemically distinct habitats. Branchipolynoe pettiboneae (Annelida: Polynoidae) is a commensal polynoid scale worm that inhabits the gill cavity of bathymodioline mussels, representing one of the dominant macrobenthic taxa widely distributed across hydrothermal vents and cold seeps in the Northwest Pacific. This species exhibits a lecithotrophic developmental mode, a trait generally considered to confer limited dispersal potential. However, the genetic diversity and biogeographic patterns of this commensal species remain poorly understood due to limited sampling. To address this knowledge gap, we performed the first population connectivity study of B. pettiboneae based on 95 individuals collected from two hydrocarbon seeps and four hydrothermal vents in the Northwest Pacific. Notably, the Haima seep and the Iheya North Original vent are the southwesternmost and northeasternmost of the six sampling sites, respectively, and are separated by over 2,000 km. Using assembled mitochondrial genomes, we conducted population genetic analyses and revealed that B. pettiboneae (1) exhibits significant genetic differentiation in the Haima seep population compared with the other five populations, (2) potentially underwent a recent demographic expansion, and (3) is subject to pervasive purifying selection across its mitochondrial protein-coding genes. These findings suggest that geographic isolation, rather than habitat types, might be the main driver of genetic differentiation of B. pettiboneae, while pervasive purifying selection underscores the conservation of mitogenome in extreme environments. This work provides a genetic foundation for future studies using higher-resolution genomic data to better elucidate the population connectivity and environmental adaptation of commensal species in extreme deep-sea habitats.