Problems with Characterizing the Protostome-Deuterostome Ancestor

Problems with Characterizing the Protostome-Deuterostome Ancestor by Paul Nelson and Marcus Ross.

Abstract:

"Since Darwin’s time, the origins and relationships of the bilaterian animals have remained unsolved problems in historical biology (Conway Morris 2000).

One of the central difficulties is characterizing the common ancestor of the protostomes and deuterostomes.

We argue that an unresolved conceptual puzzle has plagued the many attempts to describe this Urbilaterian, or, in Erwin and Davidson’s (2002) terminology, the protostome-deuterostome ancestor (PDA).

Any organism sophisticated enough to be a realistic candidate for the PDA, with such characters as an anterior-posterior axis, gut, and sensory organs, must itself have been constructed by a developmental process, or by what we term an ontogenetic network (Ross and Nelson 2002).

But the more biologically plausible the PDA becomes, as a functioning organism within a population of other such organisms, the more it will tend to “pull” (in its characters) towards one or another of the known bilaterian groups. As this happens, and the organism loses its descriptive generality, it will cease to be a good candidate Urbilaterian."

Comments by Dr. Nelson:

"... the poster focused on an unsolved conceptual problem arising from data familiar to any developmental biologist or evo-devo theorist. Only a handful of biologists (e.g., Eric Davidson; see below) currently are trying to solve the problem, which deserves to be much better known."

In the Drosophila system, the anterior-posterior (A-P, or head-to-tail) and dorsal-ventral (D-V, or back-to-front) axes of the egg (body plan) are specified in the mother’s ovary. For instance, Mom deposits bicoid mRNAs at the anterior pole of the egg. After fertilization, these mRNAs will be translated into DNA-binding proteins, which will then diffuse along a gradient towards the posterior pole of the egg.

The diffusion of bicoid begins the process (or is an important aspect, anyway) of specifying the body plan of the fly. The events occur in a single large cell, the syncitium. Cellularization –- the formation of cells within the syncitium –- is yet to come.

But not all insects establish their body plans this way. In some wasps, for instance, studied by Miodrag Grbic and Michael Strand, complete celluarization is the first noteworthy event. That is, the embryo divides into two (and then many more) distinct cells immediately, in what is known as holoblastic cleavage. "Initial cleavage events in these tiny eggs differ from the canonical type of insect syncytial cleavage. [The] wasps undergo total (holoblastic) cleavage in which nuclear division is immediately followed by cytoplasmic division, forming individual cells (blastomeres)" (Grbic 2003, p. 635).

Here's the problem. If we suppose that the syncitial developmental architecture is primitive for long germ-band insects, as is widely accepted, then how did complete cellularization evolve in some wasps? In particular, if the segmentation cascade requires the diffusion of maternal transcription factors throughout the syncitium, what would happen if a cell membrane suddenly arose in the path of those diffusing morphogens?

The celluarized environment of the C. floridanum [a wasp] embryo violates the most important paradigm of Drosophila patterning: Initiation of the segmentation cascade begins with the diffusion of transcription factors in a syncytial environment. Even though C. floridanum lacks a syncytial stage, it still undergoes long germ-band development. ...

Early cellularization of the C. floridanum egg, however, makes it unlikely that protein gradients could form by diffusion as occurs during syncytial cleavage in other long germ-band species....embryonic cells become dye uncoupled at the very beginning of embryogenesis and no syncytial stage ever exists during germ-band formation. (Strand and Grbic 1997, p. 140)

"Dye uncoupled" refers to experiments where Grbic and Strand injected early blastomeres with a dye smaller in molecular dimensions than the bicoid protein.

The dye stayed in the injected blastomere and not did not diffuse. If the dye couldn't get past the cell membrane, then it is likely that the bicoid protein couldn't either.

Reviewing these fundamental differences, Grbic muses, "It is hard to conceptualize the evolution of a novel stage that disrupts one of the crucial paradigms of Drosophila development, maternal specification of the embryonic axis" (Grbic 2003, p. 640).

These are differences of developmental architecture just within Insecta. As one moves to large groups -- e.g., the phyla, or the superphylum Ecdysozoa -- the differences becomes much more dramatic…

"Classical authors…and those of their successors who have attempted to deal with more than one embryonic form, have been struck by the amazing variety in the modes of embryonic development that exist in the various phylogenetic reaches of the Animal Kingdom… All embryos do indeed achieve the imposition of spatial patterns of differential gene expression, and yet some begin this process by intercellular interaction, and others even before there are any cells that could carry out such interactions; some rely on lineages that are autonomously committed to given functions from the moment they appear, others deal wholly in plastic, malleable cell fate assignments; some utilize eggs that before fertilization are cytoskeletally organized in both axes, some in one axis only, some apparently in neither; for some kinds of embryos every individual has a different cell lineage, while for others development depends on a set of rigidly reproducible canonical cell lineages; and some embryos display truly amazing regulative capacities….the differences among taxa in their modes of embryonic development are anything but trivial and superficial (certain hopeful reductionist delusions of recent years to the contrary)." [Davidson, 1990, pp. 365-66]

If one assumes that two (or more) taxa showing divergent early development share a common ancestor, then one has prima facie evidence that early development can vary dramatically.

In his plenary lecture at Calgary, for instance, Brian Hall said (I’ll paraphrase), ‘Once upon a time the neo-Darwinians thought that early development was functionally constrained, and thus unlikely to vary much. Now of course we know better: We’ve got hundreds of examples of divergent early development.’ What Hall didn’t show (because, to my knowledge, it doesn’t exist) was experimental evidence showing heritable changes in such characters as cleavage patterns or modes of gastrulation.

[Note: PZ Myers drew what he calls a “crude triploblastic worm.” It would be relatively easy, he argued, for this organism to vary so that it would qualify as a reasonable PDA (protostome-deuterostome ancestor)... problems arise as soon as one tries to put flesh on the bones of the [PZ Myers'} hypothesis. Suppose the crude worm were something like known flatworms. A flatworm egg wants to turn into a flatworm, with its gut, muscles, germ line, sensory organs, and epidermis in more or less the right place –- and not something else. (I would say the constraints we see in developing organisms are a generic feature of causally asymmetric systems, where entrenched upstream features govern downstream consequences...)]

It [this problem] existed for Darwin and it exists today. The problem will either be solved or it will persist. I predict it will persist, and will worsen, because of the conceptual and evidential difficulties outlined in the poster.

Dr. Nelson's References:

Britten, Roy J. and Davidson, Eric. 1971. Repetitive and non-repetitive DNA sequences and a speculation on the origins of evolutionary novelty. Quarterly Review of Biology 46:111-131.

Davidson, Eric. 1990. How embryos work: a comparative view of diverse modes of cell fate specification. Development 108:365-389.

Grbic, Miodrag. 2003. Polyembryony in parasitic wasps: evolution of a novel mode of development. Int. J. Dev. Biol. 47:633-642.

Strand, Michael and Miodrag Grbic. 1997. The Development and Evolution of Polyembryonic Insects. Current Topics in Developmental Biology 35:121-159.