Another blow to the conserved gene order in Annelida: Evidence from mitochondrial genomes of the calcareous tubeworm genus Hydroides

Mitochondrial genomes are frequently applied in phylogenetic and evolutionary studies across metazoans, yet they are still poorly represented in many groups of invertebrates, including annelids. Here, we report ten mitochondrial genomes from the annelid genus Hydroides (Serpulidae) and compare them with all available annelid mitogenomes. We detected all 13 protein coding genes in Hydroides spp., including the atp8 which was reported as a missing gene in the Christmas Tree worm Spirobranchus giganteus, another annelid of the family Serpulidae. All available mitochondrial genomes of Hydroides show a highly positive GC skew combined with a highly negative AT skew – a feature consistent with that found only in the mitogenome of S. giganteus. In addition, amino acid sequences of the 13 protein-coding genes showed a high genetic distance between the Hydroides clade and S. giganteus, suggesting a fast rate of mitochondrial sequence evolution in Serpulidae. The gene order of protein-coding genes within Hydroides exhibited extensive rearrangements at species level, and were different from the arrangement patterns of other annelids, including S. giganteus. Phylogenetic analyses based on protein-coding genes recovered Hydroides as a monophyletic group sister to Spirobranchus with a long branch, and sister to the fan worm Sabellidae. Yet the Serpulidae + Sabellidae clade was unexpectedly grouped with Sipuncula, suggesting that mitochondrial genomes alone are insufficient to resolve the phylogenetic position of Serpulidae within Annelida due to its high base substitution rates. Overall, our study revealed a high variability in the gene order arrangement of mitochondrial genomes within Serpulidae, provided evidence to question the conserved pattern of the mitochondrial gene order in Annelida and called for caution when applying mitochondrial genes to infer their phylogenetic relationships.