Reconstruction of the ancestral metazoan genome reveals an increase in genomic novelty

Abstract

Understanding the emergence of the Animal Kingdom is one of the major challenges of modern evolutionary biology. Many genomic changes took place along the evolutionary lineage that gave rise to the Metazoa. Recent research has revealed the role that co-option of old genes played during this transition, but the contribution of genomic novelty has not been fully assessed. Here, using extensive genome comparisons between metazoans and multiple outgroups, we infer the minimal protein-coding genome of the first animal, in addition to other eukaryotic ancestors, and estimate the proportion of novelties in these ancient genomes. Contrary to the prevailing view, this uncovers an unprecedented increase in the extent of genomic novelty during the origin of metazoans, and identifies 25 groups of metazoan-specific genes that are essential across the Animal Kingdom. We argue that internal genomic changes were as important as external factors in the emergence of animals.

Fig. 1

Reconstruction of ancestral genomes. Evolutionary relationships of the major groups included in his study. Different categories of HG are indicated in each node, from top to bottom, Ancestral HG, Novel HG, Novel Core HG, and Lost HG. Values assume sponges as the sister group to other animals, and placozoans as sister group to Planulozoa (=Cnidaria + Bilateria); alternative phylogenetic hypotheses are explored in Supplementary Data 3-8. Organism outlines from phylopic.org and the authors

Fig. 2

Novelty in ancestral genomes. a Proportion of Novel HG in the Ancestral HG for different holozoan ancestors. b Percentage of Core HG that are novel, and percentage of highly preserved genes among the Novel HG across different LCA. c Number of Protein Class GO hits for the fruit fly representatives of the Novel HG for the various phylogenetic nodes