Slime moulds don’t play by the rules

I’m starting to think dictyostelids are seriously interesting. These are the guys whose eerily animal-like epithelial tissues prompted the idea of multicellularity being ancestral to the lineage containing animals, choanoflagellates, fungi and amoebae. (Incidentally, Parfrey and Lahr [2013] wrote a nice critical response to that hypothesis – it deserves a post of its own, but not this post.) They are used as model organisms in (evolutionary) developmental biology (Schaap, 2011), a field which is mostly dominated by animals and plants for obvious reasons.

Recently I wrote about the developmental hourglass pattern, which means that the most conserved developmental stages are not the earliest (as Karl von Baer thought at the dawn of comparative embryology), but some way into development. This pattern has been found in several animal phyla both at the morphological level and in various features of developmental gene expression, and it was recently also discovered in plants, which prompted my first post about it.

A group of researchers reckoned they should check how universal the hourglass is, and they thought the slime mould/social amoeba and honoured developmental model organism Dictyostelium is a good place to look (Tian et al., 2013). Unlike plants and animals, which develop from a single cell, the multicellular life stage of dictyostelids is a gathering of thousands of previously independent cells that may not be genetically identical. Therefore, these tiny creatures represent a very different approach to development from our favourite lab animals. Whether or not they still show an hourglass pattern could give clues about the deeper laws that govern all developmental processes.

Dictyostelids turn out to be complete deviants in this respect. Comparisons of the genes two species of Dictyostelium use in their multicellular development show neither von Baer’s “funnel” pattern of similarity nor an hourglass. If you include single-celled stages that aren’t, strictly speaking, “developmental”, similarities of gene expression give a “reverse hourglass” with lowest similarity in the middle. If you only consider the actual multicellular developmental stages, conservation increases towards the end – an “inverted funnel”. Other measures gave Tian et al. largely consistent results – genes expressed later in development were more likely to also be present in the other species, and their sequences were more similar on average.

Now that we have a pattern – what could explain it? The authors speculate that an idea that had been used to explain the hourglass in animals may apply just as well to the inverted funnel of slime moulds. This idea is that the evolvability of a developmental stage depends on the interactions that occur during it. The more interactions between genes/cells/tissues, the worse the effect of a tiny screw-up and the smaller the chance of a beneficial change, hence the most interconnected developmental stages will tend to be most conserved in evolution.

In animals, goes the reasoning, early development is relatively simple, and later development is relatively modular. Early on, there’s less to screw up, whereas later, every screw-up is limited to part of the embryo. In between is the sweet spot where everything talks to everything and a small modification can have large knock-on effects. The result is the hourglass. In slime moulds, however, that later stage when the developing organism is subdivided into semi-independent modules never comes. All tissues keep communicating and affecting each other right up to the point where the multicellular body is fully developed. Thus, if you like, only the first half of the hourglass happens in these creatures.

It’s an interesting idea. I like it.

***

References:

Parfrey LW & Lahr DJG (2013) Multicellularity arose several times in the evolution of eukaryotes. BioEssays advance online publication, 11/01/2013, doi: 10.1002/bies.201200143

Schaap P (2011) Evolutionary crossroads in developmental biology: Dictyostelium discoideum. Development 138:387-396

Tian X et al. (2013) Dictyostelium development shows a novel pattern of evolutionary conservation. Molecular Biology and Evolution advance online publication 16/01/2013, doi: 10.1093/molbev/mst007

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