Illuminating the Base of the Annelid Tree Using Transcriptomics

Abstract

Annelida is one of three animal groups possessing segmentation and is central in considerations about the evolution of different character traits. It has even been proposed that the bilaterian ancestor resembled an annelid. However, a robust phylogeny of Annelida, especially with respect to the basal relationships, has been lacking. Our study based on transcriptomic data comprising 68,750-170,497 amino acid sites from 305 to 622 proteins resolves annelid relationships, including Chaetopteridae, Amphinomidae, Sipuncula, Oweniidae, and Magelonidae in the basal part of the tree. Myzostomida, which have been indicated to belong to the basal radiation as well, are now found deeply nested within Annelida as sister group to Errantia in most analyses. On the basis of our reconstruction of a robust annelid phylogeny, we show that the basal branching taxa include a huge variety of life styles such as tube dwelling and deposit feeding, endobenthic and burrowing, tubicolous and filter feeding, and errant and carnivorous forms. Ancestral character state reconstruction suggests that the ancestral annelid possessed a pair of either sensory or grooved palps, bicellular eyes, biramous parapodia bearing simple chaeta, and lacked nuchal organs. Because the oldest fossil of Annelida is reported for Sipuncula (520 Ma), we infer that the early diversification of annelids took place at least in the Lower Cambrian.

Re-evaluating the phylogeny of Sipuncula through transcriptomics

“…In addition, 10 taxa were chosen as outgroups from which 3 were collected live for this study (Baseodiscus unicolor, Argonomertes australiensis and Chaetopterus sp. ); 3 transcriptomes were retrieved from Riesgo et al (2012; Chiton olivaceus, Hormogaster samnitica and Octopus vulgaris); 2 transcriptomes were retrieved from GenBank (Owenia fusiformis and Magelona johnstoni), and 2 transcriptomes were provided directly by Weigert et al (2014; Eurythoe complanata and Paramphinome jeffreysii).…”

“…The public archive used was NCBI. Transcriptomes marked with ⁄ were directly provided by Weigert et al (2014) …”

“…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.…”

“…Second, with evidence of adult sipunculans in the Lower Cambrian (Huang et al, 2004), and the oldest annelid fossil representatives (Weigert et al, 2014), it appears that at least one unsegmented annelid body plan has persisted for the past 520 Myr. In this context, the morphogenetic origin, or loss, of segmentation within Annelida is a mystery that will continue to stimulate research on body plan evolution.…”

“…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.…”