Early evolution of animal cell signaling and adhesion genes

Abstract

In stark contrast to the rapid morphological radiation of eumetazoans during the Cambrian explosion, the simple body plan of sponges (Phylum Porifera) emerged from the Cambrian relatively unchanged. Although the genetic and developmental underpinnings of these disparate evolutionary outcomes are unknown, comparisons between modern sponges and eumetazoans promise to reveal the extent to which critical genetic factors were present in their common ancestors. Two particularly interesting classes of genes in this respect are those involved in cell signaling and adhesion. These genes help guide development and morphogenesis in modern eumetazoans, but the timing and sequence of their origins is unknown. Here, we demonstrate that the sponge Oscarella carmela, one of the earliest branching animals, expresses core components of the Wnt, transforming growth factor beta, receptor tyrosine kinase, Notch, Hedgehog, and Jak/Stat signaling pathways. Furthermore, we identify sponge homologs of nearly every major eumetazoan cell-adhesion gene family, including those that encode cell-surface receptors, cytoplasmic linkers, and extracellular-matrix proteins. From these data, we infer that key signaling and adhesion genes were in place early in animal evolution, before the divergence of sponge and eumetazoan lineages.

Fig. 1.

An introduction to the sponge, O. carmela. (a) Phylogenetic position of O. carmela (asterisk) relative to model bilaterians. O. carmela belongs to one of the earliest branching phyla of animals and may provide insight into the biology and genome of the first multicellular animals. (b) Macroscopic view of O. carmela overgrowing a standard brick (shown for scale). As an adult, O. carmela has no body axes and no differentiated structures other than epithelia. (c and d) Electron micrographs of the larval epithelium of O. carmela demonstrate that it has closely apposed cells (c) and a basement membrane (d, arrowheads), a feature thought to be exclusive to eumetazoans and the sponge clade containing Oscarella, the homoscleromorph sponges. Dd, D. discoideum; Sc, Saccharomyces cerevisiae; Sp, Schizosaccharomyces pombe; Oc, O. carmela; Dm, Drosophila melanogaster; Ce, Caenorhabditis elegans; Gg, Gallus gallus; Mm, Mus musculus; Hs, Homo sapiens. (Scale bars, 500 nm.)