Animal egg as evolutionary innovation: a solution to the “embryonic hourglass” puzzle

Abstract

The evolutionary origin of the egg stage of animal development presents several difficulties for conventional developmental and evolutionary narratives. If the egg's internal organization represents a template for key features of the developed organism, why can taxa within a given phylum exhibit very different egg types, pass through a common intermediate morphology (the so-called "phylotypic stage"), only to diverge again, thus exemplifying the embryonic "hourglass"? Moreover, if different egg types typically represent adaptations to different environmental conditions, why do birds and mammals, for example, have such vastly different eggs with respect to size, shape, and postfertilization dynamics, whereas all these features are more similar for ascidians and mammals? Here, I consider the possibility that different body plans had their origin in self-organizing physical processes in ancient clusters of cells, and suggest that eggs represented a set of independent evolutionary innovations subsequently inserted into the developmental trajectories of such aggregates. I first describe how "dynamical patterning modules" (DPMs) associations between components of the metazoan developmental-genetic toolkit and certain physical processes and effects may have organized primitive animal body plans independently of an egg stage. Next, I describe how adaptive specialization of cells released from such aggregates could have become "proto-eggs," which regenerated the parental cell clusters by cleavage, conserving the characteristic DPMs available to a lineage. Then, I show how known processes of cytoplasmic reorganization following fertilization are often based on spontaneous, self-organizing physical effects ("egg-patterning processes": EPPs). I suggest that rather than acting as developmental blueprints or prepatterns, the EPPs refine the phylotypic body plans determined by the DPMs by setting the boundary and initial conditions under which these multicellular patterning mechanisms operate. Finally, I describe how this new perspective provides a resolution to the embryonic hourglass puzzle.

A set of simple cell processes are sufficient to model spiral cleavage

“…Arenicola and Nereis) are not closer to each other in the parameter space than to the patterns of other, more phylogenetically distant, species. This suggests that the underlying developmental parameters are relatively easy to change ( presumably a small number of mutational changes are required) (Newman, 2011).…”

Dynamical patterning modules in plant development and evolution

“…Even though the DPM framework proposed by Newman and Bhat (Newman and Bhat, 2009;Newman, 2011) is in principle applicable to all multicellular organisms, plant development has features that suggest the presence of additional or different sets of DPMs and perhaps even a different DPM-GRN relationship. In particular, we note that many plants are characterized by having open, indeterminate development during which new tissues and organs are added continuously over the course of their life times.…”

“…Because DPMs only come into play in animal embryos when a critical number of cells have been generated (e.g., at the morula or blastula stage), it has been suggested that disparate autonomous patterning processes that may occur in the eggs of subphylum taxa serve mainly to set the initial and boundary conditions for DPM implementation, with conservation of DPM-determined "phylotypic" body plans (Newman, 2011). However, because of the immobility of plant cells, an autonomous patterning mechanism like FCW would be expected to have more profound consequences for plant body plan organization, placing it more in the DPM category.…”

“…Together, the DTFs and the DPM-associated molecules and pathways constitute what Carroll (2001) has called the "developmental toolkit". In the case of animals, the gene products enabling the DPMs are an "interaction toolkit" (Newman, 2011), which includes molecules such as cadherins, collagen, Notch, Wnt, Hedgehog and BMP. In postulating a framework in which the interplay between DPMs and DTF-associated GRNs provided the (Archaea and Bacteria) and the five major eukaryotic photoautotrophs, collectively referred to as "plants" (euglenoids, dinoflagellates, rhodophytes, chlorobionta and stramenopiles).…”

“…Given that plants and animals are different developmentally in many ways, the nature and role of any DPM operating in plants likely differ from those described for animals by Newman and Bhat (Newman and Bhat, 2009;Newman, 2011). In particular, plant DPMs must incorporate physical limitations on plant development that differ from those that prevail during animal development.…”