Mitochondrial Genome and Nuclear Sequence Data Support Myzostomida As Part of the Annelid Radiation

Abstract

The echinoderm symbionts Myzostomida are marine worms that show an enigmatic lophotrochozoan body plan. Historically, their phylogenetic origins were obscured due to disagreement about which morphological features are evolutionarily conserved, but now most morphological evidence points to annelid origins. In contrast, recent phylogenetic analyses using different molecular markers produced variable results regarding the position of myzostomids, but all suggested these worms are not derived annelids. To reexamine this issue, we analyzed data from nuclear genes (18S rDNA, 28S rDNA, Myosin II, and Elongation Factor-1alpha), and a nearly complete myzostomid mitochondrial genome. Here, we show that the molecular data are in agreement with the morphological evidence that myzostomids are part of the annelid radiation. This result is robustly supported by mitochondrial (gene order and sequence data) and nuclear data, as well as by recent ultrastructural investigations. Using Bayes factor comparison, alternative hypotheses are shown to lack support. Thus, myzostomids probably evolved from a segmented ancestor and gained a derived anatomy during their long evolutionary history as echinoderm symbionts.

A PCR survey of Hox genes in the myzostomid Myzostoma cirriferum

“…Myzostomids share signatures with annelids (e.g., Lox5, see details above) and a member of the PG 2 (Mci_pb) has been identified, which might have been lost in the platyhelminth lineage. The present findings can be interpreted as a (weak) support of the annelid affinity hypothesis and is hence in concordance with morphology and mitochondrial data (Bleidorn et al 2007). In addition, these first available Hox genes sequences for myzostomids form a starting point for future studies on their ontogeny, relative to their putative phylogenetic relationships.…”

“…The phylogenetic position of myzostomids is still under discussion and most analyses either recover an annelid or platyzoan relationship (Bleidorn et al 2007;Dunn et al 2008). Hox genes have been repeatedly used for phylogenetic inference (e.g.…”

“…Whereas the presence of many morphological characters is congruent with an annelid affinity (e.g., parapodia-like structures, chitinous chaetae, a ladder-like nervous system, trochophora larva, serial nephridia), some recent molecular analyses point to a platyzoan (Platyhelminthes and relatives) origin of these organisms (Eeckhaut et al 2000;Dunn et al 2008). However, a recent analysis using mitochondrial gene order and sequence data strongly supports an annelid affinity of Myzostomida (Bleidorn et al 2007). Nevertheless, myzostomids show a unique mode of development and the relationship of segment formation in myzostomids (Jägersten 1940) to segment formation, as described for various annelids remains unclear.…”

Arctic-boreal sibling species ofParanaitis(Polychaeta, Phyllodocidae)

“…Since we in most cases are unaware of the gene order, mutation rate will not be the same across the group we study if there has been a gene order rearrangement. In the present case this may not be a problem, because the gene order seems to be very conserved in Annelida (Bleidorn et al 2007). Another more serious objection is that the calibration is based on annelids from hydrothermal vents, and mutation rates in hydrothermal annelids may be very different from those living in more 'normal' habitats.…”

Lophotrochozoan relationships and parasites. A snap-shot

“…These analyses place myzostomids within Platyzoa & Zrzavy et al (2001) erected a new taxon called Promastigozoa uniting myzostomids with Syndermata (rotifers and acanthocephalans) -a clade that was mainly supported by spermatozoan ultrastructural characters and 18S data. This hypothesis was re-investigated by Bleidorn et al (2007), who found strong support for an annelid affinity of myzostomids based on mitochondrial sequence data, mitochondrial gene order, and myosin II heavy-chain gene data. Besides the case of the myzostomids, parasitism evolved many times in annelids.…”