Understanding animal evolution: The added value of sponge transcriptomics and genomics

After our recent discussion of the (bilaterian, i.e. 2-sided symmetry) scallop genome, it seems appropriate for these GEITP pages to go deeper into evolution of the animal kingdom — to the sponge genome — which is among the non-bilaterian taxa (Placozoa, Cnidaria, Ctenophora, and Porifera = sponge), having NO two-sided symmetry. The question therefore is: does the sponge genome and transcriptomics exhibit any “origin” of “body plan” genes that are important in Bilaterians (e.g. axial polarity, symmetry, nervous system, muscles, and even the beginning of germ layers and the gut)? As you can see from studying the attached article, the answer is YES.

The first genomes of non-bilaterian species appeared between 2005 and 2010: the cnidarian (Nematostella vectensis, a coelenterate), the placozoan (Trichoplax adhaerens, a balloon-shaped marine animal that certainly competes for the earliest ancestor of animals), the demosponge (Amphimedon queenslandica, most common sponge, having a soft body covering a hard skeleton made of calcium carbonate), and the lobate ctenophore (Mnemiopsis leydii, a comb jelly). But, in order to discover the “last common ancestor of animals” (and to trace back the early evolution of molecular, cellular, and morphological characters) — knowing the relative phylogenetic position of these non-bilaterian phyla becomes important.

The debate about which of these two phyla — sponges or comb jellies — is evolutionarily earlier, has been going on over more than a decade. Porifera (sponges) are more diverse, having >8500 species described, compared with ~200 species for ctenophores); yet, the genomes sequenced (to date) do not reflect this diversity. According to recent phylogenetic and phylogenomic studies, sponges exist within four classes: (Demospongiae, Hexactinellida, Calcarea, and Homoscleromorpha) — each with very different ecological, embryological, and morphological characteristics.

Authors [see attached article and editorial] show that the four classes of sponge have vastly different genome sizes and gene content. Authors found that the four major signaling pathways (WNT, TGFβ, Hedgehog, and Notch) — genes needed for maintenance of pluripotent stem cells and sex-cell differentiation, and the main transcription-factor families — are present in sponge, meaning that most of the “bilaterian developmental molecular toolkit” appears already in the sponge genome. Also, sponges often have a lower number of gene copies or gene types, in a given family, as compared to cnidarians and bilaterians; these data strongly support the likelihood that sponge is the most primitive of these three animal groups.

Fellow GEITP-ers are welcome to search this publication for “your favorite gene family.” Transcriptomic and genomic analyses performed so far, although still incomplete, have already revealed an important molecular disparity among the four sponge classes, which emphasizes the need to develop not only one, but ideally four, sponge models for evo-devo (relationship between evolution and developmental biology), functional, and physiological studies. Another result of these comparative gene surveys is that gene inventories alone fail to explain anatomical and physiological features of sponges and their differences, as compared with other animals. As a consequence, gene inventories must be performed — in combination with functional approaches — in order to resolve the present discrepancy between the gene presence and/or gene absence and their assumed corresponding anatomical features. Standing back on the mountaintop, these GEITP pages vote for placozoa being evolutionarily earlier 😊 than either sponges or comb jellyfish. ☹

DwN

BioEssays Aug 2018; 40, 1700237

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