Hourglasses everywhere

Ever since the theory of evolution “evolved” centuries ago, scientists have known that evolution and development are somehow related. In his Origin of Species, Charles Darwin devoted pages to the discussion of this relationship. Ill-fated theories like Haeckel’s infamous biogenetic law aside, the idea is still alive and well – in fact, it’s the foundation for the discipline of evolutionary developmental biology or evo-devo. (Yay!)

Now, the fact that embryos of related (or even seemingly unrelated) animals are often more similar than their adults has been known for a long time. But exactly what pattern these similarities follow throughout embryogenesis is a slightly more contentious issue. You might expect that embryos would start out more similar and accumulate differences as they grow into their different adult forms. But, at least for some well-studied animal groups including vertebrates, that doesn’t seem to be the case. Instead, the embryos start out pretty different, then become more similar until they reach a point of maximum resemblance (called the phylotypic stage, where the characteristic body plan of the phylum is established), and finally begin to diverge again.

(Below: two competing views of developmental evolution. Image from Irie and Kuratani (2011) via PhysOrg.

 

The original debate over whether phylotypic stages existed involved only the morphology of the embryos, but nowadays, everyone is sequencing everything, and the funnel vs. hourglass debate also moved on to a molecular level. About a couple of years ago, two papers in the same issue of Nature reported the discovery of the hourglass in the transcriptomes – the set of active genes – of two very different kinds of animals.

Kalinka et al. (2010) showed that the embryos of six fruit fly species activate the most similar set of genes at the same developmental stage where arthropod embryos in general look most similar to one another. Using a different approach, Domazet-Lošo and Tautz (2010) determined that zebrafish embryos express the oldest genes at the (vertebrate) phylotypic stage. Genes that only evolved recently are mainly active in the earliest and latest stages of development, and sexually active adults express the youngest genes. (For a proper discussion of these studies, head over to The Panda’s Thumb for Steve Matheson’s lovely posts on them.)

Thus, genes offer an independent line of evidence for the existence of the embryonic hourglass. If the embryos themselves didn’t give a clear answer, perhaps two different kinds of genetic evidence offer a more persuasive argument. Not to mention that the evidence just keeps piling up. Irie and Kuratani (2011) compared gene expression in embryos of four distantly related vertebrate species, which is a direct comparison across ten times more evolutionary time than the fly study – and once again, the hourglass was there, with its waist sitting right at the traditional phylotypic stage. Clearly, there is something about this stage that acts to preserve it over hundreds of millions of years of evolution in animals with wildly different lifestyles and reproductive habits.

And, perhaps, there is something about the phylotypic stage that compels it to evolve again and again. The most recent “transcriptomic hourglass” study isn’t about animals at all – it’s about plants. As far as anyone knows, plants evolved multicellularity and embryos completely independently of animals. Yet here’s an unassuming little plant, the plant geneticists’ workhorse Arabidopsis thaliana, with a beautiful transcriptomic hourglass eerily like that of the animals.

(Below: Arabidopsis not looking like the most important plant in science, from Wikipedia.)

Quint et al. (2012) more or less did the same thing Domazet-Lošo and Tautz did with their zebrafish, calculating the age of the genes expressed at seven different developmental stages in baby Arabidopsis. They also estimated how fast each gene evolved by comparing their sequences to some close relatives of A. thaliana. They found that the oldest and most conservative genes were expressed somewhere in mid-embryogenesis. It was undoubtedly an hourglass.

The result is all the more interesting because plants don’t have an obvious developmental hourglass in terms of morphology. Quint and colleagues observe that different land plants don’t actually differ all that much as embryos, and the divergence of their adult appearances begins well after the waist of the transcriptomic hourglass. What’s going on here? Do animals and plants have transcriptomic hourglasses for different reasons? The authors of the plant paper also note that in both animals and plants, it’s mostly the young genes that account for the transcriptome age variation throughout development. The old genes are on from start to finish. On top of them, one set of young genes is activated early on, then they are switched off and you’re left with the old “phylotypic transcriptome”, then another set of young genes is turned on. That would indicate that the hourglass is really something plants and animals have in common, but I think a lot more embryos must grow into adults before someone figures out exactly what this means…

***

References

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

Irei N & Kuratani S (2011) Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis. Nature Communications 2:248

Kalinka AT et al. (2010) Gene expression divergence recapitulates the developmental hourglass model. Nature 468:811-814

Quint M et al. (2012) A transcriptomic hourglass in plant embryogenesis. Nature advance online publication 05/09/2012, doi:10.1038/nature11394

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