Phylogenomic analyses unravel annelid evolution

Abstract

Annelida, the ringed worms, is a highly diverse animal phylum that includes more than 15,000 described species and constitutes the dominant benthic macrofauna from the intertidal zone down to the deep sea. A robust annelid phylogeny would shape our understanding of animal body-plan evolution and shed light on the bilaterian ground pattern. Traditionally, Annelida has been split into two major groups: Clitellata (earthworms and leeches) and polychaetes (bristle worms), but recent evidence suggests that other taxa that were once considered to be separate phyla (Sipuncula, Echiura and Siboglinidae (also known as Pogonophora)) should be included in Annelida. However, the deep-level evolutionary relationships of Annelida are still poorly understood, and a robust reconstruction of annelid evolutionary history is needed. Here we show that phylogenomic analyses of 34 annelid taxa, using 47,953 amino acid positions, recovered a well-supported phylogeny with strong support for major splits. Our results recover chaetopterids, myzostomids and sipunculids in the basal part of the tree, although the position of Myzostomida remains uncertain owing to its long branch. The remaining taxa are split into two clades: Errantia (which includes the model annelid Platynereis), and Sedentaria (which includes Clitellata). Ancestral character trait reconstructions indicate that these clades show adaptation to either an errant or a sedentary lifestyle, with alteration of accompanying morphological traits such as peristaltic movement, parapodia and sensory perception. Finally, life history characters in Annelida seem to be phylogenetically informative.

Genomic data do not support comb jellies as the sister group to all other animals

“…We investigated whether previous studies supporting Ctenophora-sister were conducted using adequately fitting substitution models. Using three exemplar datasets, which we call Ryan-Choano, Moroz-3D, and Whelan-6-Choano (details are provided below and in Methods), we compared the relative fit of site-homogeneous and siteheterogeneous models using Bayesian cross-validation (36, 37), a routine statistical technique used to evaluate the predictive performance of a probabilistic model, which has been commonly used in the context of phylogenetics (23,24,(38)(39)(40)(41). Using 10 cross-validation replicates, we found that in all cases, site-heterogeneous models fit these data significantly better than the site-homogeneous models that previous studies mostly relied upon ( Table 1).…”

Combining phylogenomic and supermatrix approaches, and a time-calibrated phylogeny for squamate reptiles (lizards and snakes) based on 52 genes and 4162 species

“…For example, large-scale sequencing projects have been undertaken for many important clades, in which hundreds of loci are sequenced (e.g. Dunn et al, 2008;Regier et al, 2010;Kocot et al, 2011;Chiari et al, 2012;Struck et al, 2011;Jarvis et al, 2014;Weigert et al, 2014). Yet, at the same time, most species in many clades may still have data for no more than a few genes each (see below).…”

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.…”

“…The systematic community has necessarily progressed from candidate genes through EST-based methods to 454 and Illumina-based transcriptome and genome datasets to resolve major relationships among the animal phyla (e.g., Dunn et al, 2008;Hejnol et al, 2009;Nosenko et al, 2013;Ryan et al, 2013;Moroz et al, 2014). Long outstanding issues have been resolved for within-phylum relationships among arthropods, molluscs, and annelids, to mention just some of the largest animal phyla (e.g., Meusemann et al, 2010;Kocot et al, 2011;Smith et al, 2011;Struck et al, 2011;von Reumont et al, 2012;Andrade et al, 2014;Weigert et al, 2014). A third wave now focuses on resolving lower-level phylogenetic questions, relying almost entirely on Illumina-based technology (e.g., Johnson et al, 2013; Kocot et al, 2013;Wheat and Wahlberg, 2013;Dell'Ampio et al, 2014;Fernández et al, 2014aFernández et al, , 2014b.…”