Embracing Uncertainty in Reconstructing Early Animal Evolution

Abstract

The origin of metazoans, one of the major transitions in evolution, remains mysterious. While many key aspects of metazoan origins can be reconstructed by comparing living organisms within a robust phylogenetic framework, uncertainty regarding the evolutionary relationships among sponges, ctenophores and the remainder of metazoan diversity has proven to be a major barrier. Comparative morphology and some phylogenomic analyses support the view that sponges represent the sister lineage to the rest of the metazoans, while other competing phylogenomic analyses strongly support ctenophores, a phylum of carnivorous, gelatinous marine organisms, as the sister lineage. Here, we explore why different phylogenomic studies yield different answers and discuss the implications of the two alternative hypotheses for understanding the origin of metazoan multicellularity. Reconstruction of ancient evolutionary radiations, like the one that gave rise to metazoans, is devilishly difficult and will likely require broader sampling of sponge and ctenophore genomes, improved analytical strategies, and critical analyses of the phylogenetic distribution and molecular mechanisms underlying apparently conserved traits. Rather than staking out positions in favor of the ctenophore-sister or the sponge-sister hypothesis, we submit that research programs aimed at understanding the biology of the first metazoans should embrace the uncertainty surrounding early metazoan evolution in their experimental designs.

The Origin of Animal Multicellularity and Cell Differentiation

“…The collar complex is inferred to have been present in the Urchoanozoan, and to be a choanozoan synapomorphy. The relationships among sponges (Porifera), ctenophores and other animals are depicted as a polytomy to reflect uncertainties regarding their order of divergence (King and Rokas 2017). Species silhouettes are from PhyloPic (http://phylopic.org).…”

Neuromuscular organization of the Ctenophore Pleurobrachia bachei

“…These conditions lead to numerous controversies about the early evolution of animals in general, and the origins of neurons and muscles in particular (Moroz, ). The exact phylogenetic position of Ctenophora has been extensively debated over the last decade (Alamaru, Hoeksema, van der Meij, & Huchon, ; Arcila et al, ; Borowiec, Lee, Chiu, & Plachetzki, ; Cavalier‐Smith, ; Dunn, Leys, & Haddock, ; Feuda et al, ; Halanych, Whelan, Kocot, Kohn, & Moroz, ; King & Rokas, ; Moroz et al, ; Nielsen, ; Ryan et al, ; Shen, Hittinger, & Rokas, ; Simion et al, ; Telford, Moroz, & Halanych, ; Whelan et al, ; Whelan, Kocot, & Halanych, ; Whelan, Kocot, Moroz, & Halanych, ). However, the most recent models of evolution and interdisciplinary data argue strongly that Ctenophora is a sister group to all extant Metazoa including nerveless sponges, which are morphologically simpler than comb jellies (Arcila et al, ; Moroz et al, ; Shen et al, ; Whelan et al, ).…”

Inherent forms and the evolution of evolution

“…This metazoan attachment complex is present throughout the animal phyla, including the earliest diverging and morphologically simplest, basal metazoans, the sponges (Porifera), and the best-studied extant member of the phylum Placozoa, Trichoplax adherens. However, the ctenophores-"comb jellies"-a group of organisms that is an outlier of the metazoans in several respects (King & Rokas, 2017;Lanna, 2015;Whelan et al, 2017) employ a different transmembrane domain than that of the classical cadherins (Belahbib et al, 2018).…”