Single origin and convergent host use of hexactinellid sponge symbiosis in Hesionidae (Annelida: Polychaeta) with descriptions of two new deep-sea species

Abstract Symbiotic associations between annelids and sponges are widespread and have evolved repeatedly across diverse families. However, their evolutionary history within Hesionidae remains poorly understood. Using the manned submersible Shinkai 6500, we conducted in situ observations and collected hesionid specimens from a hexactinellid sponge on the Getsuyo Seamount, north-west Pacific Ocean. An integrative taxonomic approach combining morphology and molecular phylogenetics revealed that they belong to two new species, Dalhousiella yabukii sp. nov. and Leocratides watanabeae sp. nov. Phylogenetic analyses suggest that sponge symbiosis in Hesionidae originated once, in the common ancestor of Dalhousiella and Leocratides. Nevertheless, the two new species are not each other’s closest relatives; instead, they form independent sister-clades, each including different congeners. Specimens of the two new species inhabited the same sponge host and probably shared similar ecological niches, suggesting convergent ecological specialization toward the limited resource of hexactinellid sponges in the deep sea. Such niche overlap and convergent evolution between closely related symbiotic species have not been previously reported in Hesionidae. Our findings shed new light on the origin and diversification of sponge symbiosis in Hesionidae and highlight the importance of integrative taxonomy and direct in situ observation for understanding deep-sea biodiversity.