Assessing the root of bilaterian animals with scalable phylogenomic methods

Abstract

A clear picture of animal relationships is a prerequisite to understand how the morphological and ecological diversity of animals evolved over time. Among others, the placement of the acoelomorph flatworms, Acoela and Nemertodermatida, has fundamental implications for the origin and evolution of various animal organ systems. Their position, however, has been inconsistent in phylogenetic studies using one or several genes. Furthermore, Acoela has been among the least stable taxa in recent animal phylogenomic analyses, which simultaneously examine many genes from many species, while Nemertodermatida has not been sampled in any phylogenomic study. New sequence data are presented here from organisms targeted for their instability or lack of representation in prior analyses, and are analysed in combination with other publicly available data. We also designed new automated explicit methods for identifying and selecting common genes across different species, and developed highly optimized supercomputing tools to reconstruct relationships from gene sequences. The results of the work corroborate several recently established findings about animal relationships and provide new support for the placement of other groups. These new data and methods strongly uphold previous suggestions that Acoelomorpha is sister clade to all other bilaterian animals, find diminishing evidence for the placement of the enigmatic Xenoturbella within Deuterostomia, and place Cycliophora with Entoprocta and Ectoprocta. The work highlights the implications that these arrangements have for metazoan evolution and permits a clearer picture of ancestral morphologies and life histories in the deep past.

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.…”

“…Nextgeneration sequencing (NGS) now enables us to generate large data sets for many species at a relatively low cost. 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).…”

Acoelomorpha: earliest branching bilaterians or deuterostomes?

“…Subsequent uncontaminated ribosomal RNA analyses placed Xenoturbella surprisingly among the deuterostomes (Paps et al 2009b;Philippe et al 2007;Bourlat et al 2003). However, later phylogenomic studies including EST data suggested Xenoturbella to be a sister group of Acoelomorpha together forming the sister group to the rest of bilaterians (Hejnol et al 2009).…”

“…This study considered four different lines of evidence: mitochondrial protein coding genes, nuclear-coding phylogenomic analyses (a subset of the genes used by Hejnol et al 2009), microRNA content, and the absence/ presence of the gene Rsb66. All these datasets provided weak evidence for the deuterostome affiliation of Acoelomorpha and Xenoturbella.…”

“…The authors argued that the reason for the low statistical support on the phylogenetic position of acoels was their level of missing data. However, in a follow-up study that included substantially more data, acoelomorphs (acoels and nemertodermatids) were recovered as a sister group to the rest of Bilateria with relatively strong nodal support (Hejnol et al 2009) (Table 1). Thus, different types of molecular data, from single gene and multigene phylogenies to qualitative characters, appeared to support the position of acoelomorphs as the sister group of the remaining Bilateria.…”