Pharyngula embryos become evo-devo superstars

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(Nat Commun, March 2011) Gene expression analysis of early embryos explores the most conserved stages in vertebrate development.

Vertebrates have diversified shockingly during evolution (think of a goldfish and a rhinoceros). And for that reason, it is even more stunning how similar their embryos look during development. A recent article by Naoki Irie and Shigeru Kuratani at the RIKEN Center for Developmental Biology in Japan may bring us a little closer to understanding the mechanism behind early (1).

Most biologists are familiar with Haeckel’s pithy summary of development in evolutionary context: “ontogeny recapitulates phylogeny” – the idea that animal embryos progressively resemble the various evolutionary ancestors of a given species (phylogeny) as they progress through development (ontogeny). This also apply to humans. Although you now look like a person, in the womb you looked like a fish, a tadpole and a mouse at various stages of gestation. This was a handy idea, because it explained how lineages with shared ancestry would have embryos that look so much alike.

But Haeckel’s axiom has been somewhat dismissed from the tenets of modern evolutionary developmental (or “evo-devo”) biology. Instead, it is thought that early development is conserved because mutations that cause even the slightest tinkering at this stage can have lethal consequences, and are strongly selected against. In other words, early embryonic development may follow the old adage “if it ain’t broken don’t fix it”. ┬áThat said, there is still some contention among experts about which are the most conserved developmental stages. Based on , two hypotheses have emerged: the “funnel” model proposes that the strongest developmental conservation will occur during the earliest stages of development, whereas the “hourglass” model places the highest conservation at slightly later stages, when is in full swing.

As Irie and Kuratani explain in their article, if animal development is the progressive generation of specialized cell types from a single cell, we can think of developmental conservation as similarities in the formation of equivalent cell types across species. In turn, they argue, conservation in the development of equivalent cell types across species should result in more similar embryo-wide gene expression profiles.

Using , Irie and Kuratani profiled the of embryos from four vertebrate species (mouse, chicken, frog and zebrafish) at different stages of early development. By performing an all-to-all pairwase comparison of the transcriptomes, the authors observed a clear tendency for pairs of to be more highly correlated. In fact, pharyngula embryos were more highly correlated than all other developmental stages. More importantly, because early developmental stages showed less similarity, the authors conclude that their data support the hourglass over the funnel model of developmental conservation. Moreover, based on a preliminary analysis including transcriptional data from mosquito embryos, the authors argue that such conservation may extend to all animals.

Why conserve the transcriptomes of pharyngula embryos and not earlier stages? As Irie and Kuratani rightly point out, this observation may only be revealing the process of evolution rather than a particular adaptation that has been strongly selected for (). They argue that the regulatory networks needed to build the basic bilateral body plan may be very sensitive to perturbation and contstrained by prior regulatory states.

Further research will likely answer this question. In the meantime, it is fascinating that Irie and Kuratani could detect any transcriptional conservation at all. They worked at a very low spatial resolution, trying to capture the formation of relatively scarce cell types against the background of whole embryos. Since the same are often recycled in a combinatorial and context-specific manner to instruct the formation of diverse tissues, it is rather surprising that they could pick up statistically significant signal amid all that “crosstalk”.

But they did, and that’s remarkable.

(1) Irie N and Kuratani S. Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis. Nat Commun, 2011;2:248. doi:10.1038/ncomms1248.

 

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In evolutionary biology, ‘conservation’ refers to things that were maintained unaltered (conserved) between lineages. Thus, developmental conservation means processes and mechanisms occurring during the development of an organism that also occur in organisms from either a closely or distantly related species (such as goldfish and rhinoceros).
Comparative morphology is a branch of biology that seeks to establish evolutionary relationships (or lack thereof!) by comparing anatomical structures of organisms. The central idea is that if two organisms (or organs) share an evolutionary ancestor, they will be morphologically very similar.
As implied by its name, organogenesis refers to the process of organ formation. Embryos typically go through an initial phase of growth, during which cells divide several times and form rather shapeless masses of cells that look mostly alike (at least on the outside!). At some later point, however, cells begin reorganizing, moving around and changing their shape, giving rise to structures that start resembling functional organs (gut, nervous system, hearts, etc).
“Microarrays” refer to a technique that researchers use to simultaneously measure the abundance of thousands of RNA molecules present in a sample.
Transcriptome is the name given to the collection of all the RNA transcripts present in a given biological sample at a given time. By analogy, a ‘genome’ is the collection of all genes, a ‘proteome’ is the collection of all proteins, etc.
The pharyngula stage applies specifically to vertebrate embryos. By this stage, vertebrate embryos look very similar and have developed some very important features of the vertebrate body plan: a rudimentary spinal cord, a tail, gills and, most notably, the precursor of a dorsal spine.
Bilateral comes from “bilateral symmetry” and refers to the fact that there is only one plane of ‘symmetry’ for a given organism (quotation marks intended). How many ways can you cut yourself through such that both halves are roughly identical? One – a plane that goes from head to toes and between your eyes. Note that the halves you obtain are not fully ‘symmetrical’ – some organs (heart, pancreas, liver) would only be found on one side. By contrast, there are animals with radial symmetry (sea stars, jellyfish, etc).
Sometimes, biological phenomena we observe today are not solely the result of natural selection. There are many neutral or even potentially maladaptive traits in organisms that have been conserved because there was no other way forward for evolution – something that the experts call “evolutionary constraints”. What Irie and Kuratani say is that the conservation of gene expresion in the pharyngula stage may not have been selected because it conferred an adaptive advantage, but because it was an unavoidable consequence of how vertebrate development had been structured up to that point (the ‘mechanics’ of vertebrate development).
Genes do many things. Often, genes will activate or inhibit the activity of other genes, which in turn, will activate or inhibit other genes, and so forth… Experts refer to these cascades of genes regulating each other and culminating in a given biological process or mechanism as ‘genetic pathways’.

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