MicroRNAs resolve an apparent conflict between annelid systematics and their fossil record

Abstract

Both the monophyly and inter-relationships of the major annelid groups have remained uncertain, despite intensive research on both morphology and molecular sequences. Morphological cladistic analyses indicate that Annelida is monophyletic and consists of two monophyletic groups, the clitellates and polychaetes, whereas molecular phylogenetic analyses suggest that polychaetes are paraphyletic and that sipunculans are crown-group annelids. Both the monophyly of polychaetes and the placement of sipunculans within annelids are in conflict with the annelid fossil record-the former because Cambrian stem taxa are similar to modern polychaetes in possessing biramous parapodia, suggesting that clitellates are derived from polychaetes; the latter because although fossil sipunculans are known from the Early Cambrian, crown-group annelids do not appear until the latest Cambrian. Here we apply a different data source, the presence versus absence of specific microRNAs-genes that encode approximately 22 nucleotide non-coding regulatory RNAs-to the problem of annelid phylogenetics. We show that annelids are monophyletic with respect to sipunculans, and polychaetes are paraphyletic with respect to the clitellate Lumbricus, conclusions that are consistent with the fossil record. Further, sipunculans resolve as the sister group of the annelids, rooting the annelid tree, and revealing the polarity of the morphological change within this diverse lineage of animals.

Cnidarian microRNAs frequently regulate targets by cleavage

“…Interestingly, only two miRNAs seem to be shared among the three cnidarian groups, compared to 31 ancestral miRNA families in bilaterians ( Fig. 1D; Sperling et al 2009). Notably, not only the mature sequences of these two miRNAs are conserved, but sequence homology can also be found in their hairpin structure (Fig.…”

A critical appraisal of the use of microRNA data in phylogenetics

“…Similarly, the acoels (Symsagittifera, Hofstenia) and Xenoturbella are central to the study by Philippe et al (20). The relationships among these taxa strongly contradict relationships based on traditional phylogenetic analyses, but again were excluded from the Tarver et al (8) (21), and also the key Nereis and Phascolosoma taxa from Sperling et al (22). Tarver et al (8) neither discuss the rationale for the taxon sampling in their analysis, nor justify their decision to exclude key taxa from the revised dataset.…”

“…At the time of our analysis, these included five formal phylogenetic analyses of miRNA data focused on identifying the phylogenetic position of turtles within amniotes (19), acoelomorph flatworms within animals (20), lampreys within vertebrates [hagfish and jawed vertebrates (18)], myzostomidan worms within bilaterians (21), and on establishing the monophyly of-and resolving relationships within-annelids (22). [Several additional studies discuss the phylogenetic implications of miRNA data, but do not subject these data to a formal phylogenetic analysis.…”

“…The miRNA study by Sperling et al (22) used "standard" (Wagner) parsimony-in which gains and losses of miRNA families incur equal cost (28)-and the remaining four studies (18)(19)(20)(21) used Dollo parsimony (29). Dollo parsimony allows for the unique evolution of a character and its subsequent loss (both with equal cost), but precludes reevolution of the same character (with effectively infinite cost) once it has been lost.…”

“…Bilaterian dataset. Helm et al (21) sought to resolve the phylogenetic affinity of myzostomid worms using an expanded version of the miRNA dataset from the Sperling et al (22) (Fig. 1B).…”