Extensive gene rearrangements in the mitogenomes of congeneric annelid species and insights on the evolutionary history of the genus Ophryotrocha

Abstract

Background Annelids are one the most speciose and ecologically diverse groups of metazoans. Although a significant effort has been recently invested in sequencing genomes of a wide array of metazoans, many orders and families within the phylum Annelida are still represented by a single specimen of a single species. The genus of interstitial annelids Ophryotrocha (Dorvilleidae, Errantia, Annelida) is among these neglected groups, despite its extensive use as model organism in numerous studies on the evolution of life history, physiological and ecological traits. To compensate for the paucity of genomic information in this genus, we here obtained novel complete mitochondrial genomes of six Ophryotrocha species using next generation sequencing. In addition, we investigated the evolution of the reproductive mode in the Ophryotrocha genus using a phylogeny based on two mitochondrial markers (COXI and 16S rDNA) and one nuclear fragment (Histone H3). Results Surprisingly, gene order was not conserved among the six Ophryotrocha species investigated, and varied greatly as compared to those found in other annelid species within the class Errantia. The mitogenome phylogeny for the six Ophryotrocha species displayed a separation of gonochoric and hermaphroditic species. However, this separation was not observed in the phylogeny based on the COX1, 16S rDNA, and H3 genes. Parsimony and Bayesian ancestral trait reconstruction indicated that gonochorism was the most parsimonious ancestral reproductive mode in Ophryotrocha spp. Conclusions Our results highlight the remarkably high level of gene order variation among congeneric species, even in annelids. This encourages the need for additional mitogenome sequencing of annelid taxa in order to properly understand its mtDNA evolution, high biodiversity and phylogenetic relationships.

Morphological convergence and adaptation in cave and pelagic scale worms (Polynoidae, Annelida)

“…elegans conform to this putative Polynoidae ground pattern (Fig. 1 b), and to a large extent, so does G. jameensis, differing only by the position of two tRNAs, which are generally more labile 34 . Similarly, this Polynoidae ground pattern was also found in the polynoid Polyeunoa laevis McIntosh, 1885, adding validity to the idea of a conserved gene order ground pattern in Polynoidae 35 .…”

“…In Annelida, this speculation has led to the suggestion of a common ground pattern across Errantia and Sedentaria 30 – 32 . However, recent increases in mitogenome sampling across phyllodocid lineages (i.e., Syllidae, Aphroditiformia) showed that mitochondrial gene orders are more variable than previously anticipated 25 , 30 , 33 , 34 . In Aphroditiformia, Zhang et al 25 recovered six different mitochondrial gene orders from their sampling of 16 scale worms, four being from within Polynoidae.…”

Molecular Phylogeny of Thoracotreme Crabs Including Nine Newly Determined Mitochondrial Genomes

“…The level of gene order rearrangement in mitogenomes differs among animal groups. For example, the gene order of annelids shows considerable variation even within a single genus (Tempestini et al, 2020; Sun et al, 2021), whereas brachyurans show relatively stable arrangements that are shared among families (Tan et al, 2018). The gene order of Thoracotremata in a single family is often the same with some exceptions, such as Dotillidae (three dotillids in Kobayashi et al, 2021), Pinnotheridae (six pinnotherids in Sun et al, 2022), and Xenograpsidae (two xenograpsids in Wang et al, 2021).…”

Mitogenome of a stink worm (Annelida: Travisiidae) includes degenerate group II intron that is also found in five congeneric species

“…The gene order of a mitogenome is relatively conserved; the order is sometimes the same among higher taxa, e.g., across orders of annelids, when considering only protein-coding genes (PCGs) 3 . Conversely, the gene order in some marine invertebrates, including annelids, shows an intra-familial variation 2 , 5 – 9 and may shed light on the phylogenetic relationships of relatively closely related taxa.…”