Annelid phylogeny and the status of Sipuncula and Echiura - PubMed
- ️Mon Jan 01 2007
Annelid phylogeny and the status of Sipuncula and Echiura
Torsten H Struck et al. BMC Evol Biol. 2007.
Abstract
Background: Annelida 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.
Results: Sipuncula, Echiura, Siboglinidae, and Clitellata are all nested within polychaete annelids according to phylogenetic analyses of three nuclear genes (18S rRNA, 28S rRNA, EF1alpha; 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.
Conclusion: Using 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.
Figures

ML analysis and BI of Nuc data set with 81 OTUs (-ln L = 66,627.30). 1 of 2 best trees is shown. In the other tree the trichotomy of Nephtyidae, Syllidae, and Pilargidae is resolved with Syllidae being sister of Nephtyidae. OTUs with just the genus names (e.g., Lumbricus) indicate that the sequences from different species of that genus were concatenated. Nuc consisted of 9,482 characters, from which 4,552 (28S rRNA – 2,504; 18S rRNA – 1,375; EF1α – 673) unambiguously aligned and non-saturated ones were included. BS values above 50 shown at the branches on the left; PP's on the right or alone. The branch leading to Ophryotrocha labronica is reduced by 90%. Ophryotrocha individuals have been sampled from a long time culture, which got bottlenecked several times. For 28S rRNA, Capitella forms a long branch and does not cluster with the two other Capitellidae in the analyses. ML settings: Base frequencies: A = 0.2727, C = 0.2495, G = 0.2586, T = 0.2192; Rate matrix: AC, AT, CG, GT = 1.0000, AG = 2.5097, CT = 3.7263; α = 0.4830; Proportion of invariant sites = 0.3103. Models in BI: 28S rRNA, 18S rRNA, EF1α : GTR+I+Γ. Clitellata, Echiura, Siboglinidae, Sipuncula highlighted with gray and bars indicate polychaete groups: orange = outgroup; A, blue = Aciculata; C, green = Canalipalpata; S, red = Scolecida; Ca = Capitellida; Eu = Eunicida; Ph = Phyllodocida; Sa = Sabellida; Sp = Spionida; Te = Terebelliformia; Aph = Aphroditiformia.

ML analysis and BI of NucMt data set with 10 OTUs and only nucleotides (-ln L = 29,951.42). OTUs with just the genus names (e.g., Lumbricus) indicate that the sequences from different species of that genus were concatenated. NucMt consisted of 16,351 characters with 11,454 unambiguously aligned and non-saturated (in addition to Nuc: COX1 – 489; 16S rRNA – 463; 18S rRNA – 406; CYTB – 365; COX3 – 258; COX2 – 219; NAD6 – 118; ATP8 – 32). BS values shown at upper position right to node; PP's in the middle; 1-p of AU test at lower position. ML settings: Base frequencies: A = 0.2536, C = 0.2243, G = 0.2498, T = 0.2723; Rate matrix: AC = 2.3662, AG = 4.2648; AT = 2.0966, CG = 2.5643, CT = 6.7166, GT = 1.0000; α = 0.4824; Proportion of invariant sites = 0.3555. Models in BI: 28S rRNA, 12S rRNA: GTR+I+Γ ; 18S rRNA: K80+I+Γ ; EF1α = F81+I+Γ ; 16S rRNA, CYTB: GTR+Γ ; ATP8, COX1-3, NAD6 = F81+Γ. Clitellata, Echiura, Siboglinidae, Sipuncula highlighted with gray and bars indicate polychaete groups: orange = outgroup; A, blue = Aciculata; C, green = Canalipalpata; S, red = Scolecida.
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