Inherency of Form and Function in Animal Development and Evolution

Abstract

I discuss recent work on the origins of morphology and cell-type diversification in Metazoa – collectively the animals – and propose a scenario for how these two properties became integrated, with the help of a third set of processes, cellular pattern formation, into the developmental programs seen in present-day metazoans. Inherent propensities to generate familiar forms and cell types, in essence a parts kit for the animals, are exhibited by present-day organisms and were likely more prominent in primitive ones. The structural motifs of animal bodies and organs, e.g., multilayered, hollow, elongated and segmented tissues, internal and external appendages, branched tubes, and modular endoskeletons, can be accounted for by the properties of mesoscale masses of metazoan cells. These material properties, in turn, resulted from the recruitment of “generic” physical forces and mechanisms – adhesion, contraction, polarity, chemical oscillation, diffusion – by toolkit molecules that were partly conserved from unicellular holozoan antecedents and partly novel, distributed in the different metazoan phyla in a fashion correlated with morphological complexity. The specialized functions of the terminally differentiated cell types in animals, e.g., contraction, excitability, barrier function, detoxification, excretion, were already present in ancestral unicellular organisms. These functions were implemented in metazoan differentiation in some cases using the same transcription factors as in single-celled ancestors, although controlled by regulatory mechanisms that were hybrids between earlier-evolved processes and regulatory innovations, such as enhancers. Cellular pattern formation, mediated by released morphogens interacting with biochemically responsive and excitable tissues, drew on inherent self-organizing processes in proto-metazoans to transform clusters of holozoan cells into animal embryos and organs.

Interplay of mesoscale physics and agent-like behaviors in the parallel evolution of aggregative multicellularity

“…Many of the genes involved in generic processes in animal and plant lineages predated or accompanied the emergence of multicellularity. In those lineages, morphogenesis and pattern formation can be characterized in terms of the dynamical patterning modules (DPMs) that mobilize specific physical forces and physicochemical effects to produce the respective structural motifs [39,45,46]. Similarly, some gene products that shape dictyostelids and myxobacteria as multicellular materials were carried over from single-celled ancestors, as were some gene products involved in agent behaviors.…”

“…An important implication of the perspective we have presented here is that physics-based and agent-based approaches to understanding development are not simply alternative modeling or computational strategies, but represent realities of complex biological systems that are represented to various extents in different organismal lineages. Thus, the material nature of multicellular systems and the inherent structural motifs entailed by the relevant physics introduces a predictability to morphological evolution [45,47]. In contrast, agent-type behaviors are more unconstrained and open-ended in their possibilities, and their evolution could have led phylogenetic lineages that embody them (e.g., vertebrates, which have the novelty of a neural crest [181]) in less predictable directions.…”

“…Despite continually changing their neighbors, subunits of non-living liquids cohere due to the weakly attractive electronic interactions that hold them together. The cells of developing animal tissues also remain cohesive despite their translocation, but for a different reason: the homophilic attachment proteins (classical cadherins) that mediate their transient attachment extend through the cells' membranes to form stable connections between adhesive and motile functions [45]. In plant and fungal tissues, instead of the charge-based or covalent bonds of the atomic or molecular subunits of non-biological solids, the cells are cemented together by pectins and glycoproteins which are subject to unique forms of reversible remodeling [39,46].…”

“…Animal tissues during early stages of development, as noted above, behave in important ways like non-living liquids. As development proceeds, however, some tissues undergo a transformation where cell movements become constrained and the cellular mass behaves more like a solid [45]. In these tissues, solidification may provide increased mechanical integrity, and new morphological outcomes and constructional elements (e.g., exo-and endoskeletons) arise with the physical properties of these materials.…”

The origins and evolution of animal identity

“…Even more alien to much of present-day thinking is the Kantian concept of "natural purpose," which implies a recursive self-definition that seems to defy natural explanation (Moss and Newman, 2015). In this essay I argue that the concepts of natural kind, essence, and natural purpose are in fact applicable to living systems, but only if certain tenets of the modern synthesis are relinquished in favor of a "physico-genetic" perspective that emphasizes the material properties of cell assemblages and their inherent properties (Newman, 2012, Newman, 2018, Newman, 2019b. Rather than conflicting with naturalistic biological science, I propose that these concepts are necessary to it and enable an understanding of the relation between development and evolution, and organismal identity and individuality.…”