Phylogenetic evidence for the modular evolution of metazoan signalling pathways

Abstract

One contribution of 17 to a theme issue 'Evo-devo in the genomics era, and the origins of morphological diversity'. Communication among cells was paramount to the evolutionary increase in cell type diversity and, ultimately, the origin of large body size. Across the diversity of Metazoa, there are only few conserved cell signalling pathways known to orchestrate the complex cell and tissue interactions regulating development; thus, modification to these few pathways has been responsible for generating diversity during the evolution of animals. Here, we summarize evidence for the origin and putative function of the intracellular, membrane-bound and secreted components of seven metazoan cell signalling pathways with a special focus on early branching metazoans (ctenophores, poriferans, placozoans and cnidarians) and basal unikonts (amoebozoans, fungi, filastereans and choanoflagellates). We highlight the modular incorporation of intra-and extracellular components in each signalling pathway and suggest that increases in the complexity of the extracellular matrix may have further promoted the modulation of cell signalling during metazoan evolution. Most importantly, this updated view of metazoan signalling pathways highlights the need for explicit study of canonical signalling pathway components in taxa that do not operate a complete signalling pathway. Studies like these are critical for developing a deeper understanding of the evolution of cell signalling.This article is part of the themed issue 'Evo-devo in the genomics era, and the origins of morphological diversity'.

Insulin receptors and wing dimorphism in rice planthoppers

“…R. Soc. B 372: 20150489 [35][36][37][38][39][40][41][42][43][44]. Emerging evidence indicated that the IIS pathway plays a key role in determining the developmental plasticity of tissue or organs in insects [39,45].…”

Perspectives on the history of evo-devo and the contemporary research landscape in the genomics era

“…The other major sections illustrate how genomics and other approaches are being applied to gain insights into the evolutionary origins of morphological diversity. Major morphological transitions and innovations are considered first with articles on the origins of animal multicellularity from a classical perspective by Cavalier-Smith [52] and illustrating the impact of genomics by Babonis & Martindale [20] and an article on the evolution of land plants by Harrison [53]; the major transition that created the unique mammalian middle ear is discussed by Tucker [46]. The next section focuses on diversification and modifications of morphology as exemplified by tetrapod limbs by Saxena et al [54], flowers by Pam Soltis and co-workers [55], cranial shape in birds by Abzhanov and co-workers [45] and wing coloration patterns in butterflies by Jiggins et al [56].…”

“…As they point out, duplications of whole genomes allow complex intergenic interactions and therefore have the potential to produce greater morphological diversity than single-gene duplications. Another mechanism that creates new genes is by gene fusion and this is discussed in the article in this issue by Babonis & Martindale [20] in relation to the evolution of the genes that encode components of metazoan signalling pathways.…”

“…Surprisingly, it emerged that these developmental genes are evolutionarily ancient and highly conserved. Thus, for example, many of the genes encoding the main vertebrate signalling molecules were first discovered in Drosophila [18] but were subsequently found widely throughout the metazoan animal kingdom (as discussed by Babonis & Martindale [20]). Gene regulatory networks-complex networks of interactions between transcription factors and gene regulatory regionsfor example, the gene regulatory network involved in early specification in sea urchin embryos [21]-and other regulatory networks involving signalling molecules and their signal transduction pathways were also found to be highly conserved.…”

“…This conservation also suggested that evolutionary novelties arise by modification of pre-existing regulatory networks. It was also possible to begin to look at the phylogeny of developmental genes, bringing an entirely new perspective and providing a starting point for understanding the evolution of morphological differences (discussed in this issue by Holland et al [26]) and major transitions such as multicellularity (discussed in this issue by Babonis & Martindale [20]). …”