Phantom hourglasses

Holy ribosome, I’ve just written close to two thousand words about a paper. I… think I may have got a bit too excited. Or too bogged down in little technical details. Either way, you got lucky. The two-thousand word monster is not what you’re getting.

The reason I got excited about Piasecka et al. (2013) is that it, er, qualifies some other things I’d previously got excited about. And by “qualifies”, I mean turns inside out and performs a thorough autopsy on.

I previously touched upon the idea of the developmental hourglass – meaning that the embryos of related creatures are most similar to each other somewhere in the middle of development. The great rival of this hypothesis is that of early conservation (or the “funnel”), where embryos diverge from a similar starting point. The latter has been around as long as comparative embryology itself. The hourglass is a pretty intriguing pattern and raises all kinds of questions about what causes it – but of course, to have a cause, it has to exist in the first place.

So my previous excitement had been partly about the observation that the hourglass – originally noted in visible traits of embryos – also exists in the changing sets of genes activated throughout development (the transcriptome). According to various papers, genes expressed in mid-embryogenesis are on average older, slower-evolving and behave more similarly across species than genes active at other stages. If such observations are correct, that would certainly indicate that the hourglass is a real thing and something strange is going on with constraints and evolvability.

But, and here comes the Piasecka paper – is it?

This study is huge. There is (to use a highly technical phrase) a fucking shitload of stuff in it. Instead of looking at some big global property of the transcriptome, these authors went into all kinds of detail about various properties of specific sets of genes. They looked at – well, they say they looked at five different measures of evolutionary constraint, but actually some of those are made up of more than one thing, so really it’s quite a bit more than five.

And when they go down to that level of detail, they find that the hourglass is not a universal property of the developmental genetics of zebrafish embryos (unlike Domazet-Lošo and Tautz [2010] reported). Different measures of evolutionary constraint such as the strength of selection against protein-changing mutations, the age of the genes (which is what the original study focused on), or the conservation of their regulatory elements, show different patterns. There are hourglasses, there are a couple of funnels, and then there are parameters that just don’t exhibit much systematic change at all.

(There’s also a couple of points about potentially dodgy statistical approaches in some of these papers, which may make all the difference between an hourglass and a funnel. That’s a bit scary.)

I can’t say I’ve properly digested this paper. There’s an awful lot in it, and, my head was spinning non-stop when I finished reading. It’s definitely fascinating stuff, though, and once again, the conclusion is that things are More Complicated. (I’m kind of getting used to that at this point…) Before, you could look at a group of creatures, compare their development and ask, funnel or hourglass? Then you could ask why. Now, you can’t just make grand generalisations about anything. Taking Piasecka et al. at face value, “funnel or hourglass” is not even a valid question – it depends on exactly what you’re measuring. So much for “laws” of developmental evolution…

***

References:

Domazet-Lošo T & Tautz D (2010) A phylogenetically based transcriptome age index mirrors ontogenetic divergence patterns. Nature 468:815-818

Piasecka B et al. (2013) The hourglass and the early conservation models—co-existing patterns of developmental constraints in vertebrates. PLoS Genetics 9: e1003476

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