A Large and Consistent Phylogenomic Dataset Supports Sponges as the Sister Group to All Other Animals

Abstract

Resolving the early diversification of animal lineages has proven difficult, even using genome-scale datasets. Several phylogenomic studies have supported the classical scenario in which sponges (Porifera) are the sister group to all other animals ("Porifera-sister" hypothesis), consistent with a single origin of the gut, nerve cells, and muscle cells in the stem lineage of eumetazoans (bilaterians + ctenophores + cnidarians). In contrast, several other studies have recovered an alternative topology in which ctenophores are the sister group to all other animals (including sponges). The "Ctenophora-sister" hypothesis implies that eumetazoan-specific traits, such as neurons and muscle cells, either evolved once along the metazoan stem lineage and were then lost in sponges and placozoans or evolved at least twice independently in Ctenophora and in Cnidaria + Bilateria. Here, we report on our reconstruction of deep metazoan relationships using a 1,719-gene dataset with dense taxonomic sampling of non-bilaterian animals that was assembled using a semi-automated procedure, designed to reduce known error sources. Our dataset outperforms previous metazoan gene superalignments in terms of data quality and quantity. Analyses with a best-fitting site-heterogeneous evolutionary model provide strong statistical support for placing sponges as the sister-group to all other metazoans, with ctenophores emerging as the second-earliest branching animal lineage. Only those methodological settings that exacerbated long-branch attraction artifacts yielded Ctenophora-sister. These results show that methodological issues must be carefully addressed to tackle difficult phylogenetic questions and pave the road to a better understanding of how fundamental features of animal body plans have emerged.

Embracing Uncertainty in Reconstructing Early Animal Evolution

“…In the case of the metazoan controversy, analyses employing site-homogeneous models of protein evolution with partitioning (a different model for each gene) tend to recover ctenophores as the sister branch ([2, 3, 7, 32, 33, 38–40], but see [35, 42]). In contrast, analyses employing site-heterogeneous models (and in particular the CAT model [47]) typically recover sponges as the sister branch ([34–37, 41, 42], but see [38, 40, 48]).…”

Comprehensive phylogenomic analyses resolve cnidarian relationships and the origins of key organismal traits

“…In addition, the adult staurozoan body plan includes features common to both the polyp and medusa stages of other cnidarians, thus adding to their phylogenetic significance (Collins 2002(Collins , 2010Miranda, et al 2016a;Miranda, et al 2013;Miranda, et al 2016b). The phylogenetic position of staurozoans relative to other medusozoan lineages remains controversial and recent hypotheses (Kayal, et al 2013;Simion, et al 2017;Zapata, et al 2015) present different implications for the evolution of medusozoan body plans ( Figure 1F). Analyses of rDNA, life history and anatomical features have suggested that Staurozoa is the sister lineage to the remainder of Medusozoa (Collins 2002;Van Iten 1992).…”

Characterization of a group I Nme protein of Capsaspora owczarzaki—a close unicellular relative of animals

“…First, the deep phylogeny of animals is unresolved. Currently, there are two competing theories placing either sponges 48 or ctenophores 49 as the earliest-branching lineage. Second, the sequences of Nme genes and proteins often do not contain sufficient phylogenetic signal to reconstruct their evolutionary history at the base of the animal tree.…”