The making of a branching annelid: an analysis of complete mitochondrial genome and ribosomal data of Ramisyllis multicaudata

Abstract

Ramisyllis multicaudata is a member of Syllidae (Annelida, Errantia, Phyllodocida) with a remarkable branching body plan. Using a next-generation sequencing approach, the complete mitochondrial genomes of R. multicaudata and Trypanobia sp. are sequenced and analysed, representing the first ones from Syllidae. The gene order in these two syllids does not follow the order proposed as the putative ground pattern in Errantia. The phylogenetic relationships of R. multicaudata are discerned using a phylogenetic approach with the nuclear 18S and the mitochondrial 16S and cox1 genes. Ramisyllis multicaudata is the sister group of a clade containing Trypanobia species. Both genera, Ramisyllis and Trypanobia, together with Parahaplosyllis, Trypanosyllis, Eurysyllis, and Xenosyllis are located in a long branched clade. The long branches are explained by an accelerated mutational rate in the 18S rRNA gene. Using a phylogenetic backbone, we propose a scenario in which the postembryonic addition of segments that occurs in most syllids, their huge diversity of reproductive modes, and their ability to regenerate lost parts, in combination, have provided an evolutionary basis to develop a new branching body pattern as realised in Ramisyllis.

Syllidae mitochondrial gene order is unusually variable for Annelida

“…that inhabit practically all marine benthic realms (Aguado et al 2015b). Surprisingly, Aguado et al (2015a) found that the gene order of the two investigated syllids (Ramisyllis multicaudata and Trypanobia cryptica) was completely different from the ground pattern proposed for Pleistoannelida. However, since these were the first two mt genomes from syllids, the authors could not assess if Syllidae in general or only members of the more recent clade including Ramisyllis and Trypanobia show these different gene orders.…”

“…Occasionally, some genes of Streptosyllis sp., T. antoni and Typosyllis sp. end in TA or simply T. These variations from the typical stop and start codons have been also found in R. multicaudata and T. cryptica (Aguado et al 2015a), and incomplete stop codons are also present in other annelids (Bleidorn et al 2006;Li et al 2016). Interestingly, alternative start and stop codons only appear in those syllids with highly rearranged genomes (i.e.…”

“…In R. multicaudata and T. cryptica, the AT skews are positive, while GC skews negative (Aguado et al 2015a). In most studied annelids, the GC skew is usually more negative than the AT skew (Bleidorn et al 2006;Zhong et al 2008;Richter et al 2015;Li et al 2016;Patra et al 2016).…”

“…All these three taxa belong to Sedentaria. Aguado et al (2015a) analysed the first two mt genomes of Syllidae, one of the largest groups not only in Errantia, but in Annelida in general. The Syllidae currently comprises more than 700 spp.…”

“…More recently, Aguado et al (2015a;2015b) performed new molecular analyses, including more terminals when compared with previous studies (genera Alcyonosyllis, Trypanobia and Ramisyllis). All analyses agreed in recovering the family Syllidae as monophyletic, early divided into two major clades: one corresponding to the subfamily Anoplosyllinae and the other one comprising the rest of syllids.…”