Jumping through hoops: Structural rearrangements and accelerated mutation rates on Dendrodorididae (Mollusca: Nudibranchia) mitogenomes rumble their evolution

Abstract

The systematics of the family Dendrodorididae, with only three valid genera, is a challenge for integrative taxonomists. Its members lack hard structures for morphological comparisons and their mitochondrial and nuclear markers provide contradictory phylogenetic signals, making phylogenetic reconstructions difficult. This molecular discordance has been hypothesized to be the result of nuclear pseudogenes or exogenous contamination. However, these hypotheses have not been tested. Here, we assembled the first genome drafts of seven Dendrodorididae species to investigate the evolutionary processes of this family. Two of the mitogenomes displayed an identical structural rearrangement involving the translocation of three coding genes and five tRNAs, described for the first time in nudibranchs. In addition, we found particularly high dN and dN/dS values and multiple insertions and deletions on the mitochondrial genes of smooth Dendrodoris. In contrast, nuclear single-copy ortholog genes showed no such mutational differences. Models of protein structures from mitochondrial genes are conserved, suggesting conserved functionality. Phylogenies using mitogenomic and nuclear data showed that species with rearranged mitogenomes form a clade, although Dendrodorididae relationships remained unresolved. The present study provides novel evidence for accelerated mutation rates in the mitogenomes of Dendrodorididae, which presumably have implications on respiratory adaptation, and highlights the importance of using genomic data to unveil rare evolutionary processes, crucial for correctly inferring phylogenies.

Keywords: Cyto-nuclear discordance; Mollusca; Protein modeling; Systematics; dN/dS.