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genomic phylostratigraphy; macroevolution; sensory systems; vertebrates; placodes; neural crest; zebrafish
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.
