'Biogeneric' developmental processes: drivers of major transitions in animal evolution

Abstract

Using three examples drawn from animal systems, I advance the hypothesis that major transitions in multicellular evolution often involved the constitution of new cell-based materials with unprecedented morphogenetic capabilities. I term the materials and formative processes that arise when highly evolved cells are incorporated into mesoscale matter 'biogeneric', to reflect their commonality with, and distinctiveness from, the organizational properties of non-living materials. The first transition arose by the innovation of classical cell-adhesive cadherins with transmembrane linkage to the cytoskeleton and the appearance of the morphogen Wnt, transforming some ancestral unicellular holozoans into 'liquid tissues', and thereby originating the metazoans. The second transition involved the new capabilities, within a basal metazoan population, of producing a mechanically stable basal lamina, and of planar cell polarization. This gave rise to the eumetazoans, initially diploblastic (two-layered) forms, and then with the addition of extracellular matrices promoting epithelial-mesenchymal transformation, three-layered triploblasts. The last example is the fin-to-limb transition. Here, the components of a molecular network that promoted the development of species-idiosyncratic endoskeletal elements in gnathostome ancestors are proposed to have evolved to a dynamical regime in which they constituted a Turing-type reaction-diffusion system capable of organizing the stereotypical arrays of elements of lobe-finned fish and tetrapods. The contrasting implications of the biogeneric materials-based and neo-Darwinian perspectives for understanding major evolutionary transitions are discussed.This article is part of the themed issue 'The major synthetic evolutionary transitions'.

Keywords: diploblasty; liquid tissues; morphological evolution; reaction–diffusion mechanism; tetrapod limb; triploblasty.

Figure 1.

Major morphological transitions in the early history of the animals mediated by the emergence of novel biogeneric material properties. Ancestral unicellular holozoans (top row) had adhesive protocadherins and other cell surface molecules that permitted some species to form transient colonies. Certain subpopulations of these cells acquired DNA sequences specifying both Wnt, a secreted protein that induces A/B polarization, and the cytoskeleton-binding domain of the animal-specific classical cadherins. Together, these molecular novelties acted in cell aggregates to coordinate cell–cell adhesion with intracellular mechanics, constituting these clusters as cohesive ‘liquid tissues’ (second row), with the capacity to form lumens and undergo transient multilayering, forming body plans with features of present-day sponges and placozoans. Among these early emerging metazoans, some further acquired the capacity for tissue reshaping, such as elongation by convergent extension (third row, left), based on the PCP pathway elicited also by Wnt, but using novel mediators such as Vang/Stbm. Some of these organisms also acquired the ability to form stably layered sheet-like tissues (third row, right) and hence epithelial appendages, due to the presence of the novel enzyme peroxidasin which cross-links type IV collagen into a stiff, flexible basal lamina (stippling). Both PCP and a basal lamina are present in all extant eumetazoans, the morphologically simplest of which, the ctenophores and the cnidarians, are referred to together as ‘diploblasts,’ although their phylogenetic affinity is obscure. In some diploblastic forms, novel extracellular matrix molecules (galectins, TSR superfamily proteins, fibronectin) were acquired that elicited epithelial–mesenchymal transformation (EMT) in one or another of the two basic tissue layers during development, leading to an intermediate layer, the mesoblast, constituting the resulting animals as ‘triploblasts’ (fourth row; a developing bird embryo is represented). All of these triploblastic forms are bilaterally symmetric during at least part of their life cycles, possibly owing to the geometrical constraints of three-layered development, leading them to also be referred to as ‘bilaterians’. The phylogenetic affinities among many triploblastic groups and their genealogical relationships to extant diploblasts are unclear. A generalization that can be derived from this perspective is that certain major animal body plan categories have unambiguous morphological hallmarks that can be directly attributed to the material properties of their constituent tissues. These material properties, in turn, often depend straightforwardly on the consequences of the mobilization of new physical forces and effects by the products of novel genes [3,4].

Figure 2.

Gnathostome paired appendage development and hypothesized Turing mechanism for skeletal pattern formation. Early-stage embryonic limb buds (left column) and late-stage embryonic skeletons (right column) are shown for two gnathostomes, the Japanese catshark, a cartilaginous fish (top row) and the chicken, a tetrapod (bottom row). Morphogenetic toolkit molecules have been shown experimentally to interact in Turing-type reaction–diffusion networks in the limb bud mesenchyme of several tetrapod species, where they mediate patterned skeletogenesis. This suggests that ancestral fin tissues may have contained primitive versions of such networks that became ‘tuned’ over the course of evolution to generate the stereotypical limb skeletons of tetrapods. The middle column shows the results of computer simulations of a reaction–diffusion network with parameter choices showing, in principle, that the distinctive patterns of distantly related gnathostomes can be generated from a single patterning mechanism with no change in network topology [74].