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Open Access Research

Phylostratigraphic profiles reveal a deep evolutionary history of the vertebrate head sensory systems

Martin Sebastijan Šestak1, Vedran Božičević2, Robert Bakarić13, Vedran Dunjko14 and Tomislav Domazet-Lošo1*

Author Affiliations

1 Laboratory of Evolutionary Genetics, Ruđer Bošković Institute, Bijenička cesta 54, Zagreb, Croatia

2 Evolutionsbiologie, Biozentrum Abteilung II, Ludwig-Maximilians-Universität München, Großhaderner Straße 2, 82152 Planegg-Martinsried, Germany

3 Max-Planck-Institut für Evolutionsbiologie, August-Thienemannstrasse 2, 24306 Plön, Germany

4 School of Informatics, University of Edinburgh, 10 Crichton Street, EH8 9AB Edinburgh, UK

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Frontiers in Zoology 2013, 10:18  doi:10.1186/1742-9994-10-18

Published: 12 April 2013

Abstract

Background

The vertebrate head is a highly derived trait with a heavy concentration of sophisticated sensory organs that allow complex behaviour in this lineage. The head sensory structures arise during vertebrate development from cranial placodes and the neural crest. It is generally thought that derivatives of these ectodermal embryonic tissues played a central role in the evolutionary transition at the onset of vertebrates. Despite the obvious importance of head sensory organs for vertebrate biology, their evolutionary history is still uncertain.

Results

To give a fresh perspective on the adaptive history of the vertebrate head sensory organs, we applied genomic phylostratigraphy to large-scale in situ expression data of the developing zebrafish Danio rerio. Contrary to traditional predictions, we found that dominant adaptive signals in the analyzed sensory structures largely precede the evolutionary advent of vertebrates. The leading adaptive signals at the bilaterian-chordate transition suggested that the visual system was the first sensory structure to evolve. The olfactory, vestibuloauditory, and lateral line sensory organs displayed a strong link with the urochordate-vertebrate ancestor. The only structures that qualified as genuine vertebrate innovations were the neural crest derivatives, trigeminal ganglion and adenohypophysis. We also found evidence that the cranial placodes evolved before the neural crest despite their proposed embryological relatedness.

Conclusions

Taken together, our findings reveal pre-vertebrate roots and a stepwise adaptive history of the vertebrate sensory systems. This study also underscores that large genomic and expression datasets are rich sources of macroevolutionary information that can be recovered by phylostratigraphic mining.

Keywords:
Genomic phylostratigraphy; Macroevolution; Sensory systems; Vertebrates; Placodes; Neural crest; Zebrafish