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In search of what unites animal groups at the level of embryos and their genes

New research led by the Tomancak lab at the Max Planck Institute of Molecular Cell Biology and Genetics (MPI-CBG) in Dresden brings the power of modern molecular techniques to bear on a classic problem in biology: the profound connections between different animal species and the differences in how animals develop. The team also shed light on the reason why there is a period of similarity in the middle of animal embryonic development, a fundamental problem that has so far remained untackled. Analysis of the data showed that the developmental period when arthropods are most similar in form is indeed underpinned by a corresponding similarity in gene expression patterns. This discovery both confirms the conclusions of previous anatomical studies and extends our understanding of the relationship between development and evolution to the molecular level. (Nature, 9 December 2010)

A 200-year-old controversy resurrected in the 21^st century

It has long been noted that there are striking similarities between the embryonic development of animals and their evolutionary histories. This relationship between how animals develop and deep evolutionary time hints at the existence of profound connections between different animal species and has therefore captured the imagination of both biologists and the wider public.

However, ever since the first observations were discussed by leading 19^th century biologists, such as von Baer, Darwin, and Haeckel, the meaning and existence of these similarities has been fraught with controversy arising from the subjective nature of the comparisons of different animal forms. New research from an collaborative international team (Casey Bergman at the University of Manchester, Uwe Ohler at Duke University, and Pavel Tomancak at the Max Planck Institute of Molecular Cell Biology and Genetics in Dresden) led by the Tomancak lab has sought to bring the power of modern molecular techniques to bear on this classic problem in biology.

While the pioneers of embryology believed that animal species are most similar at the earliest stages of their embryonic development, the arrival of improved observational methods in the 20^th century led to a revised proposal. It was noticed that the middle periods of embryonic development exhibit the highest similarity between species belonging to the same broad taxonomic group called ‘phylum’, with earlier and later periods often showing remarkable divergence in form. Known as the hourglass model, this proposal has so far been supported by the same types of evidence available to 19^th century biologists, namely subjective comparisons of embryo appearance.

A Molecular time machine from present to deep evolutionary times

Taking advantage of advancements in large-scale gene-based methods, Dr Karolina Varga compared the embryonic development of six different fruit fly species at the molecular level of gene expression. Analysis of the data, led by Dr Alex Kalinka, showed that the developmental period when arthropods are most similar in form is indeed underpinned by a corresponding similarity in gene expression patterns. “This discovery both confirms the conclusions of previous anatomical studies and extends our understanding of the relationship between development and evolution to the molecular level,” explained Dr Kalinka.

The team also argues that they have shed light on the reason why there is a period of similarity in the middle of animal embryonic development, a fundamental problem that has so far remained untackled. “We have shown that this period of similarity between animal species is being actively preserved by natural selection as opposed to being a period that is simply resistant to change for other reasons,” explained co-author Dr Casey Bergman from the University of Manchester.

The results that were published in the December issue of Nature open up new horizons, as the species used are one of the best-studied experimental model systems. It is remarkable that the evolutionary mechanisms that led to the initial branching on the animal tree of life some 600 million years ago are still active today. Detecting the hourglass pattern among such closely related species is for biologists equivalent to obtaining a time machine, as these species are very much alive today and can be probed and studied by modern technologies such as genome manipulation and high-resolution imaging. “We hope to catch a glimpse of the processes that shaped, in deep evolutionary time, the remarkable diversity of animal forms observed today” says Pavel Tomancak about the long term goals of his research.

 

capture:

The famous Ernst Haeckel comparative analysis of vertebrate embryos constructed from Drosophila embryo images. The mosaic contains ~4000 tiles drawn from a database of 38000 images of in situ expression patterns during Drosophila embryogenesis.
image: Pavel Tomancak, MPI-CBG

original publication:

Alex T. Kalinka*, Karolina M. Varga*, Dave T. Gerrard, Stephan Preibisch, David L. Corcoran, Julia Jarrells, Uwe Ohler, Casey M. Bergman & Pavel Tomancak:
Gene expression divergence recapitulates the developmental hourglass model
Nature, December 9, 2010
doi:10.1038/nature09634

* these authors contributed equally