Embracing Uncertainty in Reconstructing Early Animal Evolution

Abstract

The origin of animals, one of the major transitions in evolution, remains mysterious. Many key aspects of animal evolution can be reconstructed by comparing living species within a robust phylogenetic framework.However, uncertainty remains regarding the evolutionary relationships between two ancient animal lineages - sponges and ctenophores - and the remaining animal phyla. Comparative morphology and some phylogenomic analyses support the view that sponges represent the sister lineage to the rest of the animals, while other phylogenomic analyses support ctenophores, a phylum of carnivorous, gelatinous marine organisms, as the sister lineage. Here, we explore why different studies yield different answers and discuss the implications of the two alternative hypotheses for understanding the origin of animals. Reconstruction of ancient evolutionary radiations 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 ctenophores-sister or the sponges-sister hypothesis, we submit that research programs aimed at understanding the biology of the first animals should instead embrace the uncertainty surrounding early animal evolution in their experimental designs.