First mitogenome-based phylogenetic analysis and divergence time estimation of deep-sea elasipodid sea cucumbers (Holothuroidea: Elasipodida)

Abstract

Elasipodida is a major deep-sea holothuroid order, and distributed across depths ranging from 350 m to 7,000 m. Its high species diversity and extensive bathymetric range make it a key model system for investigating the evolutionary processes and adaptive radiation of deep-sea fauna. The mitogenome is characterized by several advantages, such as maternal inheritance, small size, fast evolutionary rates and low recombination. Moreover, it serves as an effective molecular marker for resolving phylogenetic relationships and reconstructing divergence histories in holothuroids. However, the scarcity of complete mitochondrial genome sequences from elasipodid species has substantially hindered resolution of the phylogenetic relationships among constituent families and reconstruction of their divergence history. This study reports, for the first time, the complete mitochondrial genomes of four deep-sea elasipodid species: Laetmogone violacea , Enypniastes eximia , Psychropotes longicauda , and Benthodytes sp. The four mitogenomes exhibit substantial length variation (16,500 to 18,757 bp) while retaining the canonical metazoan gene complement of 37 genes. All four species exhibited negative AT-skew values. Amino acid composition analysis revealed a pronounced preference for leucine. Each species possesses a full set of 22 transfer RNA (tRNA) genes, including duplicated copies of trnL and trnS . Phylogenetic analyses robustly support two major clades within the order Elasipodida: the Psychropotidae–Pelagothuriidae clade and the Elpidiidae–Laetmogonidae clade. The 13 protein-coding genes exhibit identical gene order across the 18 examined holothuroid species, except for the inverse transposition of nad6 in E. eximia ; in addition, tRNA gene rearrangements were detected. Divergence time estimation indicates that the stem lineage of Elasipodida likely originated by the Middle Devonian (387 Ma), with the crown radiation of the order beginning in the Middle Permian (262.77 Ma). Collectively, this study establishes a foundational mitogenomic dataset and provide a robust scientific foundation for future studies on the temporal divergence and evolutionary history of elasipodid sea cucumbers.