Wednesday, June 10, 2009

Development Genes in the Earliest Animals

I recently discussed the earliest animals, and what the original animal might have been like. (Or rather, the originals of several purported animal clades.) A just-released paper7 has added support for my model, although it also supports several others.

Lapébie, P., Gazave, E., Ereskovsky, A., Derelle, R., Bézac, C., Renard, E., Houliston, E., & Borchiellini, C. (2009). WNT/β-Catenin Signalling and Epithelial Patterning in the Homoscleromorph Sponge Oscarella PLoS ONE, 4 (6) DOI: 10.1371/journal.pone.0005823

What this paper demonstrates is that one particular branch of the sponges, the homoscleromorphs, use one of the oldest mechanisms of controlling animal development in ways very much like much more complex animals such as insects and mammals.

The specific mechanism is the Wnt/TGF-β system, which I've also mentioned elsewhere, making the point that it's probably a more powerful calculator than is usually assumed. The Wnt system is one of those whose origins seem to go back to the beginning of animals, although it doesn't seem to be present in the choanoflagellates.10

The expression of Wnt and TGF-β in the Homoscleromorph Sponge Oscarella:
[...] showed complementary expression patterns in relation to the evenly spaced ostia (canal openings) of the exopinacoderm (ectoderm), highly reminiscent of Wnt expression during skin appendage formation in vertebrates. Furthermore, experimental activation of the Wnt/β-catenin pathway using GSK3β inhibitors provoked formation of ectopic ostia, as has been shown for epithelial appendages in Eumetazoa. We thus suggest that deployment of Wnt signalling is a common and perhaps ancient feature of metazoan epithelial patterning and morphogenesis.7

Figure 1: Complementary expression patterns of Wnt ligands in Oscarella lobularis exopinacoderm. Click on image to see full figure and original caption. (From Ref 7 figure 2.)

The homoscleromorphs have been thought to be part of a more distantly related group of sponges, the demosponges (so says Wiki as of this writing), but recent evidence is that they form a separate clade, more closely related to us than the calcareous sponges, previously thought to be the closest relatives of the eumetazoans (including us).6, 7, 8

This is particularly important to deciphering the earliest history of the animals. In Poriferan paraphyly and its implications for Precambrian palaeobiology by Sperling, Pisant, and Peterson, there is a good discussion of how we can use the paraphyly of the sponges to find the sequence of development of some of the features of the more advanced animals, the eumetazoans.

As is happens, many genes and features long thought to be absent in sponges are turning out to be present, especially in the larvae. One important feature is the ability to create epithelia with basal membranes and cell junctions capable of a water-tight seal. As it happens, all sponges can do this, but most only do it intermittently while creating spicules.20

Figure 2: Schematic of a representative epithelium. Click on image to see original caption. (From Ref 20, figure 1.)

The epithelium is extremely important in development, because it is a topological surface capable of supporting a coordinate system in which each cell has a unique location, which, in turn, can be fed into its gene expression system.

(One mechanism by which this can be, and often is, done is to set up a pair of diffusion gradients at right angles, so that each cell gets a different mix of signaling molecules. This mix can be translated, within each cell, into different ratios of transcription factors (TF's), which in turn can react differently on gene expression.36)

Another thing that can be done with an epithelium is to create regularly spaced "spots" through a mechanism involving diffusion. I'm not going to go into details here, but the results can be seen in Figure 1, and is discussed in the paper.7

As mentioned above, all the major lineages of sponge have larvae that can produce epithelia, of sorts. However:
Homoscleromorpha exhibit a true epithelial morphogenesis-morphogenetic movements of cells united with their neighbours in a layer.[ref] Epithelial folding is one of the basic morphogenetic processes reiterated throughout embryonic development in Eumetazoa. Interactions between epithelial cells and the extracellular matrix play a fundamental role in this morphogenesis.[ref] In Homoscleromorpha, this process is observed during the egg's follicle formation,[ref] during the metamorphosis in a rhagon (earliest developmental stage with a functional aquiferous system),[ref] during the sponge growth starting as formation of projections of the exopinacoderm,[ref] during asexual reproduction by budding,[ref] during ostia formation and reparative regeneration ([ref]).8

I should mention the paper the above quote comes from, My favourite animal The Homoscleromorph sponge Oscarella lobularis, a promising sponge model in evolutionary and developmental biology by Alexander V. Ereskovsky, Carole Borchiellini, Eve Gazave, Julijana Ivanisevic, Pascal Lapébie, Thierry Perez, Emmanuelle Renard, Jean Vacelet. This paper, like Lapébie et al.7 (see above) and Sperling et al.,6 (see above) offers a good discussion of the place of the Homoscleromorpha in early animal evolution.

Ereskovsky, A., Borchiellini, C., Gazave, E., Ivanisevic, J., Lapébie, P., Perez, T., Renard, E., & Vacelet, J. (2009). The Homoscleromorph sponge Oscarella lobularis, a promising sponge model in evolutionary and developmental biology BioEssays, 31 (1), 89-97 DOI: 10.1002/bies.080058

Now, let me go way back to my thoughts about the earliest animal, discussed in Ur... Ur... Ur...:
The original animal was somewhat like a larval sponge: a small ball of cells, but with differentiation and differential expression of a bunch of genes associated with developmental control in almost all animals.30, 15, 16, 31

Like sponges and choanoflagellates, it used a collared flagellum for its food, and like sponge larvae it could swim and possessed phototaxis and chemosensing abilities, able to guide its swimming based on external sensory information.16

I made the argument in Searching for the Urbilaterian that no matter what symmetry an animal has, or not, it has to know its left from its right, and its up from its down, in order to guide its activity. The same is true for phototaxis. Thus, even the larvae of sponges must have some genes differentially expressed to let cells know where they are in the body. The same almost certainly holds true for placozoans, which also have differentially expressed genes, although none have yet been proven to provide lateral directionality.37, 38, 39 [Footnotes and links have been updated.]

Thus, we have a small ball of cells, with a bunch of collared flagella, probably in front, ciliated cells along the equator, and some sort of sensory abilities.

Based on the information in these new papers, and some of the references (that I hadn't found previously), I'll add to that.

First, one of the biggest problems with the sponges as ancestors for the rest of the metazoa is the water-canal system. Most observers seem to think that it is unique enough that it must have evolved once, so it would have had to have been lost by the eumetazoans when they diverged from their common ancestor with the Homoscleromorpha. That, in turn, has prompted the idea that they evolved from a sponge larva.1

However, some larval sponges have non-functional choanocyte chambers:
The larva of many species in the class Demospongiae, the parenchymella, has also been reinterpreted recently as a post-gastrulation stage in which no inversion of layers occurs. The late stereoblastula differentiates intermingled micromeres and macromeres, followed by a selective ‘‘centrifugal migration’’ [ref] of micromeres towards the surface (Fig. 2). This long-known process has now been interpreted as gastrulation by ‘‘mixed delamination’’ [ref]. Then, cell differentiation begins to produce a solid parenchymella made of macromere-derived unciliated cells and micromere-derived ciliated cells, up to a total of 11 cell types (unpubl. obs.), occasionally including choanocytes organized into non-functional chambers. [emphasis mine]4

It's completely plausible, IMO, that a small animal like a floating sponge might have had a system of internal water-canals, while still having a regular shape and the ability to swim. Thus, each lineage would have branched off from the main line (with swimming adults), then developed a sessile lifestyle.

It may be that the swimming done by some groups of sponge larvae doesn't actually require the knowledge of left/right and up/down, at least beyond the cellular level:
The ring-cells around the posterior pole (relative to direction of motion) of the parenchyma larva of the demosponge Amphimedon has been shown to be photosensitive and to respond to blue light ([refs]). These cells effectively steer the sponge, using long cilia providing for a phototactic response.13

It may well be that there was a steady progression of advance in developmental mechanisms, with one lineage of sponges branching off after each advance. Thus, the last branch, the Homoscleromorpha, would have had almost the full suite of mechanisms, probably including biradial symmetry.

Another problem with sponges involves the spicules. These have often been thought to have evolved once, but Sperling et al. disagree:
Therefore, it is clear from the emerging sponge phylogeny that spicules arose at least three times within ‘Porifera’: at least once within Silicispongia, once within Calcispongia and once at either at the base or within Homoscleromorpha. Given the clear homoplasy of massive calcareous skeletons within demo- and calcisponges ([ref]), convergence of spicule structure as well should not be too surprising.6

Finally, let me mention communication. It seem unlikely that this animal had nerve cells (although it's been suggested23), however much of the cellular machinery needed for chemical communication is present in at least some lineages of sponges.23

For a small animal, with few fast-moving predators, chemical communication may well have been sufficient. Sponges are capable of coordinated actions across even large bodies,21 and the hexactinellid sponge Rhabdocalyptus dawsoni uses an "action potential" rather similar to that of nerve cells:
Impulses propagated at 0.27±0.1cms-1 with an absolute refractory period of 29 s and a relative refractory period of approximately 150 s.22

If this model is true, our most distant ancestor might have had a fairly sophisticated system of communication long before the invention of nerve cells. It would be directly ancestral to our modern system of chemical emotions, and may have been even more sophisticated, since there were no nerve cells to handle more "digital" types of calculation. Indeed, the chemical intelligence displayed by modern vertebrates in controlling their development may well have been used to control active behavior in this ancient ancestor.

Links: (Some of these are duplicates of links from earlier posts. Not all have been called out in the text. Many are derived from the main article. Use the back key if you came via clicking a footnote.) (I've included only the links referenced in this leader.)

1. Six major steps in animal evolution: are we derived sponge larvae?

2. A Phylogenomic Investigation into the Origin of Metazoa

3. The Protistan Origins of Animals and Fungi

4. Choanoflagellates, choanocytes, and animal multicellularity

5. Cell-Cell Adhesion in the Cnidaria: Insights Into the Evolution of Tissue Morphogenesis

6. Poriferan paraphyly and its implications for Precambrian palaeobiology

7. WNT/β-Catenin Signalling and Epithelial Patterning in the Homoscleromorph Sponge Oscarella

8. My favourite animal The Homoscleromorph sponge Oscarella lobularis, a promising sponge model in evolutionary and developmental biology

9. The Premetazoan Ancestry of Cadherins Requires free registration

10. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans

11. Early evolution of animal cell signaling and adhesion genes

12. Alternative Wnt Signaling Is Initiated by Distinct Receptors requires free registration (use Science login)

13. Evolution of sensory structures in basal metazoa

14. The Trichoplax Genome and the Nature of Placozoans

15. Wnt and TGF-β Expression in the Sponge Amphimedon queenslandica and the Origin of Metazoan Embryonic Patterning

16. Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity

17. A maternally localised Wnt ligand required for axial patterning in the cnidarian Clytia hemisphaerica

18. Review: How was metazoan threshold crossed? The hypothetical Urmetazoa

19. The last common bilaterian ancestor

20. Epithelium—The Primary Building Block for Metazoan Complexity

21. Coordinated contractions effectively expel water from the aquiferous system of a freshwater sponge

22. Impulse conduction in a sponge

23. A Post-Synaptic Scaffold at the Origin of the Animal Kingdom

24. Cytological Basis of Photoresponsive Behavior in a Sponge Larva

25. Purinergic transmission in the central nervous system

26. Size independent selective filtration of ultraplankton by hexactinellid glass sponges

27. Concatenated Analysis Sheds Light on Early Metazoan Evolution and Fuels a Modern “Urmetazoon” Hypothesis

28. Lower Cambrian Vendobionts from China and Early Diploblast Evolution

29. Molecular phylogeny of choanoflagellates, the sister group to Metazoa

30. Hox, Wnt, and the evolution of the primary body axis: insights from the early-divergent phyla

31. Emergence, development and diversification of the TGF-β signalling pathway within the animal kingdom

32. Neuroactive substances specifically modulate rhythmic body contractions in the nerveless metazoon Tethya wilhelma (Demospongiae, Porifera)

33. The left-right axis in the mouse: from origin to morphology

34. A transcriptional regulatory cascade that controls left/right asymmetry in chemosensory neurons of C. elegans

35. Key innovations, convergence, and success: macroevolutionary lessons from plant phylogeny

36. Evolution and Morphogenesis of Differentiated Multicellular Organisms: Autonomously Generated Diffusion Gradients for Positional Information

37. The Trox-2 Hox/ParaHox gene of Trichoplax (Placozoa) marks an epithelial boundary

38. The Early ANTP Gene Repertoire: Insights from the Placozoan Genome

39. The Trichoplax PaxB Gene: A Putative Proto-PaxA/B/C Gene Predating the Origin of Nerve and Sensory Cells


  1. shit man, you really know a LOT about molecular evolution and whatnot.

  2. Hello Friends,

    Development genes and evolution publish high quality reports on all aspects of development biology. Studying genes that regulate early heart development in animals, scientists have solved a puzzle about one gene's role, finding that it acts in concert with a related gene. Thanks a lot for sharing with us...