Mitochondrial and morphological adaptions of Lindaspio polybranchiata (Annelida: Spionidae) in the South China Sea

Abstract

A dense population of Lindaspio polybranchiata (Annelida: Spionidae) was discovered in a novel cold seep with drastic methane seepage located on the northern passive continental margin of the South China Sea. L. polybranchiata may function as a pioneer species by rapidly colonizing this nascent methane seep. We studied its classification status and evolutionary selection adaptation based on the mitochondrial genome. Phylogenetic analysis revealed that the deep-sea genus Lindaspio clustered with the neritic Rhynchospio aff. asiatica, and the ancestor of the deep-sea Lindaspio might originate from shallow-water spionids. Twelve potentially adaptive mutations were identified in cox1, cox3, cytb, and nad5. The morphological characteristics of L. polybranchiata and R. aff. asiatica collected in the intertidal zones were systematically compared to explore the possible phenotypic adaptations of L. polybranchiata to extreme deep-sea environments. L. polybranchiata lost its eyespots due to long-term colonization of the dark habitat in the deep sea but developed an enlarged caruncle for facilitating chemical perception in the darkness. The specific ventral branchiae and extended respiratory surfaces may aid the survival of L. polybranchiata in the hypoxic environment of the cold seep. This study provides novel insights into the molecular and morphological adaptations of a species endemic in chemosynthetic ecosystems.