Punctuated Emergences of Genetic and Phenotypic Innovations in Eumetazoan, Bilaterian, Euteleostome, and Hominidae Ancestors

Abstract

Phenotypic traits derive from the selective recruitment of genetic materials over macroevolutionary times, and protein-coding genes constitute an essential component of these materials. We took advantage of the recent production of genomic scale data from sponges and cnidarians, sister groups from eumetazoans and bilaterians, respectively, to date the emergence of human proteins and to infer the timing of acquisition of novel traits through metazoan evolution. Comparing the proteomes of 23 eukaryotes, we find that 33% human proteins have an ortholog in nonmetazoan species. This premetazoan proteome associates with 43% of all annotated human biological processes. Subsequently, four major waves of innovations can be inferred in the last common ancestors of eumetazoans, bilaterians, euteleostomi (bony vertebrates), and hominidae, largely specific to each epoch, whereas early branching deuterostome and chordate phyla show very few innovations. Interestingly, groups of proteins that act together in their modern human functions often originated concomitantly, although the corresponding human phenotypes frequently emerged later. For example, the three cnidarians Acropora, Nematostella, and Hydra express a highly similar protein inventory, and their protein innovations can be affiliated either to traits shared by all eumetazoans (gut differentiation, neurogenesis); or to bilaterian traits present in only some cnidarians (eyes, striated muscle); or to traits not identified yet in this phylum (mesodermal layer, endocrine glands). The variable correspondence between phenotypes predicted from protein enrichments and observed phenotypes suggests that a parallel mechanism repeatedly produce similar phenotypes, thanks to novel regulatory events that independently tie preexisting conserved genetic modules.

Generic and context-dependent gene modulations duringHydrawhole body regeneration

“…2B, 2C, Fig. S6), encoding orthologs of the human secreted frizzledrelated proteins (Wenger and Galliot, 2013). sFRPs can inhibit Wnt/b-catenin signaling as well as BMP signaling via BMP-1/Tolloid interactions (Lee et al, 2006;Bovolenta et al, 2008).…”

“…The negative cross-talk we identify here between Wnt/b-catenin and BMP signaling suggest that the interactions between these two signaling systems that deliver mutually exclusive positional information predate Cnidaria divergence. The origin of this cross-talk might be either unique and evolutionarily-conserved, or submitted to parallel evolution (Wenger and Galliot, 2013).…”

Injury-induced immune responses in Hydra

“…To provide a complete overview of the evolutionarily-conserved components of the Hydra innate immune system, we annotated with Panther [50] a recent extensive Hydra vulgaris transcriptome [51,52] and found 2636 transcripts related to one or several of the keywords "B-cell, T-cell, complement, defence, immune, interferon, interleukin, NF-B, Toll". The methodology is described in We also manually identified the transcripts encoding Hydra immune proteins that exhibit more divergent or taxon-specific sequences, and were thus not retained in the unbiased approach, such as matrix metalloproteinases or AMPs (see Supplementary File 3).…”

Deficient autophagy drives aging inHydra

“…Also except for the Drosophila gut, somatic tissues in adult flies and nematodes do not self-renew, while self-renewal is an essential component of homeostasis in humans. Finally, a significant proportion of human orthologous genes were lost in fly and nematodes as evidenced by their presence in cnidarians, a bilaterian sister group (Figure 1A) (Wenger and Galliot 2013;Schenkelaars et al 2017). Therefore, additional invertebrate models could be profitably developed to help discover novel genes, pathways and mechanisms relevant for human aging.…”