Evolution News and Views has an interesting article titled, Groundbreaking Paper Shows Thousands of New Genes Needed for the Origin of Animals, which reports on a recent paper by Jordi Paps and Peter W. H. Holland in Nature Communications that attempts to infer the minimal protein-coding genome of the first animal and estimate the proportion of “novelties” in the ancestral genomes. Surprisingly, the paper uncovers "an unprecedented increase in the extent of genomic novelty during the origin of metazoans."
Genomic novelty in the origin of animals. Concerning gene novelty, we infer the ancestral metazoan genome included a remarkable 1189 Novel HG [homology groups]; this number is similar to that inferred by previous study centred on the genome of a demosponge. Our analyses indicate a threefold increase compared to novelties in the previous nodes (389, 340, and 399 novel HG in the older holozoan nodes; Fig. 1, Supplementary Data 3). The Novel HG comprise 19% of the total HG in the first metazoan, compared to only 8–10% in most older nodes examined; Planulozoa and Bilateria LCA [last common ancestor] nodes also have high proportions of Novel HG (Figs. 1, 2a, Supplementary Note 3, Supplementary Data 5)… The 1189 metazoan Novel HG contain a large number of regulatory functions compared to the metazoan Ancestral HG set (e.g., 23 vs 6% transcription factors, 11 vs 4% signalling), and are depauperate in enzymatic and metabolic functions (Supplementary Data 4 and 6). Comparing the Novel HG of each phylogenetic node, the number genes for several protein classes displays a peak in the animal ancestor (Fig. 2c); the novel functions which are more abundant in the LCA of animals (Supplementary Data 6) are nucleic acid binding (23%), transcription factors (23%), and signalling molecules (11%). Thus, the first animal genome was not only showing a higher proportion of Novel HG, but these also perform major multicellular functions in the modern fruit fly genome. The implication is that the transition was accompanied by an increase of genomic innovation, including many new, divergent, and subsequently ubiquitous genes encoding regulatory functions associated with animal multicellularity.
Twenty five novel core groups of genes in animals. We identified which novel gene functions were more retained through evolution of animals. We find a total of 25 Novel Core HG: protein groups emerging in the genome of the first animal and still present in at least 43 of the 44 metazoan genomes examined (Table 1); these are independent of alternative phylogenetic scenarios at the root of animals. For these 25 HG, we give examples of modern bilaterian gene families contained in these HG. Together they cover the spectrum of classical functions linked to animal multicellularity: gene regulation, signalling, cell adhesion and cell cycle. Earlier opisthokont LCA have much lower numbers of Novel Core HG (Fig. 1, Supplementary Data 3 and 7), supporting the importance of genetic innovation in the emergence of animals.
The paper concludes:
There are two alternative scenarios that could explain these patterns depending on the length of the branch leading to the metazoan LCA [last common ancestor]. The first assumes that the birth rate of new genes was constant over time, thus the branch leading to the first metazoan was longer than other opisthokont internodes. This would imply an extended ‘stew’ in which the molecular components of animal biology were assembled. However, we note that molecular phylogenetic analyses do not generally show longer branches in the stem lineage of animals, contrary to this scenario. The second possibility involves many new genes emerging during a short ‘popcorn’ stage, caused either by a higher gene birth rate (perhaps produced by environmental factors elevating mutation rates, or due to whole-genome duplications), and/or a lower gene death rate (due to high integration of new genes into regulatory networks). In this scenario, the acquisition of multicellularity would quickly stabilise new molecular systems for cell adhesion, cell communication and the control of differential gene expression, as shown by the increase in proportion of Novel Core HG [homology group] seen in the metazoan ancestor. These include genes previously hypothesized to be pivotal in the emergence of Metazoa, with additional genes singled out here for the first time as agents involved in the transition. This scenario is also consistent with enhanced rates of gene novelty in the ancestors of Planulozoa [ctenophores, placozoans, cnidarians + bilaterians] and Bilateria when embryonic patterning systems were being elaborated. Further data and analyses are needed to discriminate between the two scenarios.
In short: 1189 homology groups are necessary for the origin of Metazoa, 494 novel HGs are required for the origin of Eumetazoa (sponges + Planulozoa + Bilateria), 1201 novel HGs are needed for the origin of Planulozoa (ctenophores, placozoans, cnidarians + bilaterians), and an additional 1580 HGs are required for the origin of Bilateria. I’m a layperson, but these numbers strike me as quite high. From an evolutionary standpoint, is there anything particularly astonishing about them?
Finally, here’s ENV’s take on the paper:
Whether you’re an evolutionary biologist or a proponent of intelligent design, the notion that the origin of animals required new genes — even numerous new genes — might strike you as uncontroversial. But this claim was strongly challenged by UC Berkeley evolutionary paleontologist Charles Marshall who reviewed Darwin’s Doubt in the journal Science. It actually became a centerpiece of the debate between Marshall and Meyer about the Cambrian explosion… Marshall didn’t stop there. He went further, saying that Meyer has an “idiosyncratic fixation with new protein folds” and “an outdated understanding of morphogenesis” — all due to Meyer’s supposedly inaccurate claims that the Cambrian explosion would have required the origin of many new genes. Now this new paper, “Reconstruction of the ancestral metazoan genome reveals an increase in genomic novelty,” provides a direct refutation of Marshall’s insistence that the origin of animals didn’t require lots of new genes.
In the opinion of readers, does the new paper at least partially vindicate Meyer? What say you?