Annelid phylogeny and the status of Sipuncula and Echiura

Abstract

BackgroundAnnelida comprises an ancient and ecologically important animal phylum with over 16,500 described species and members are the dominant macrofauna of the deep sea. Traditionally, two major groups are distinguished: Clitellata (including earthworms, leeches) and "Polychaeta" (mostly marine worms). Recent analyses of molecular data suggest that Annelida may include other taxa once considered separate phyla (i.e., Echiura, and Sipuncula) and that Clitellata are derived annelids, thus rendering "Polychaeta" paraphyletic; however, this contradicts classification schemes of annelids developed from recent analyses of morphological characters. Given that deep-level evolutionary relationships of Annelida are poorly understood, we have analyzed comprehensive datasets based on nuclear and mitochondrial genes, and have applied rigorous testing of alternative hypotheses so that we can move towards the robust reconstruction of annelid history needed to interpret animal body plan evolution.ResultsSipuncula, Echiura, Siboglinidae, and Clitellata are all nested within polychaete annelids according to phylogenetic analyses of three nuclear genes (18S rRNA, 28S rRNA, EF1α; 4552 nucleotide positions analyzed) for 81 taxa, and 11 nuclear and mitochondrial genes for 10 taxa (additional: 12S rRNA, 16S rRNA, ATP8, COX1-3, CYTB, NAD6; 11,454 nucleotide positions analyzed). For the first time, these findings are substantiated using approximately unbiased tests and non-scaled bootstrap probability tests that compare alternative hypotheses. For echiurans, the polychaete group Capitellidae is corroborated as the sister taxon; while the exact placement of Sipuncula within Annelida is still uncertain, our analyses suggest an affiliation with terebellimorphs. Siboglinids are in a clade with other sabellimorphs, and clitellates fall within a polychaete clade with aeolosomatids as their possible sister group. None of our analyses support the major polychaete clades reflected in the current classification scheme of annelids, and hypothesis testing significantly rejects monophyly of Scolecida, Palpata, Canalipalpata, and Aciculata.ConclusionUsing multiple genes and explicit hypothesis testing, we show that Echiura, Siboglinidae, and Clitellata are derived annelids with polychaete sister taxa, and that Sipuncula should be included within annelids. The traditional composition of Annelida greatly underestimates the morphological diversity of this group, and inclusion of Sipuncula and Echiura implies that patterns of segmentation within annelids have been evolutionarily labile. Relationships within Annelida based on our analyses of multiple genes challenge the current classification scheme, and some alternative hypotheses are provided.

Re-evaluating the phylogeny of Sipuncula through transcriptomics

“…First, sipunculans traditionally have been considered a distinct animal phylum (Sedgwick, 1898;Hyman, 1959;Clark, 1969;Stephen and Edmonds, 1972;Rice, 1985;Saiz-Salinas, 1993;Cutler, 1994;Valentine, 1997;Strand et al, 2010). However, a series of molecular hypotheses show accumulative support for the inclusion of sipunculans within the annelid radiation (McHugh, 1997;Boore and Staton, 2002;Struck et al, 2007;Dunn et al, 2008;Struck et al, 2011), as one of the earliest diverging annelid lineages (Dordel et al, 2010;Hejnol et al, 2009;Struck et al, 2011;Weigert et al, 2014), suggesting that Annelida should be recognized as one of the most biologically diverse clades within Spiralia http://dx.doi.org/10.1016/j.ympev.2014.10.019 1055-7903/Ó 2014 Elsevier Inc. All rights reserved.…”

Multiple origins of pelagicism within Flabelligeridae (Annelida)

“…The species used here differs from the description of F. vitjasi by having two pairs of gonopores located at the anterior margins of the fourth and fifth chaetigers instead of the single pair reported by Buzhinskaya (1977 Struck et al (2007), Rousset et al (2007), and morphology (frontal palps, prostomium on top of peristomium, most with compound neurochaetae, epidermal papillae, and large (gonadal) papillae on one to three chaetigers of the anterior eight; Banse, 1969;Rouse and Pleijel, 2001;. Only vouchered and non-redundant (specimens collected from different localities) sequences available from GenBank were included in the analysis.…”

The complete mitochondrial genome of Cephalothrix simula (Iwata) (Nemertea: Palaeonemertea)

“…Analyses of expressed sequence tags from Lineus viridis placed Nemertea in a clade together with Mollusca or with Annelida + Sipuncula (Struck and Fisse, 2008). Nemertea was placed as the sister group of Brachiopoda in a few other studies using other datasets, e.g., myosin heavy chain type II (Ruiz-Trillo et al, 2002), three combined nuclear genes (18S rRNA, 28S rRNA, and EFla) (Struck et al, 2007); concatenated nuclear, ribosomal and mitochondrial genes (Bourlat et al, 2008), and expressed sequence tags for two nemerteans (or Brachiopoda + Phoronida; Dunn et al, 2008). However, Zrzavy et al (1998Zrzavy et al ( , 2001) inferred a sister relationship between Nemertea and Sipuncula, and Giribet et al (2004) did so with Entoprocta.…”

“…Whereas none have supported a platyhelminth + nemertea clade; recent molecular analyses consistently place Nemertea within the coelomate Lophotro- chozoa, but at various positions-as sister to mollusks, brachiopods, entoprocts, etc. (e.g., Giribet et al, 2004;Turbeville and Smith, 2007;Struck et al, 2007;Bourlat et al, 2008;Dunn et al, 2008;Struck and Fisse, 2008). These findings have not been tested with nucleotide data and gene-order information from whole mitochondrial genome sequences.…”