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

Abstract

BackgroundThe 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.ResultsTo 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.ConclusionsTaken 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.

The origin and evolution of chordate nervous systems

“…This is not to say when the structure itself evolved, but only to predict when the genetic framework for a structure such as the brain evolved. For example, an analysis of genes involved in development of sensory structures in vertebrates showed that genes for the eyes, including the lens evolved first, with peaks for the number of new genes for the retina and eye evolving in deuterostomes and for the lens in cephalochordates [53]. By contrast, the peak appearances of new genes for the olfactory system, ear and lateral line as well as that for cranial placodes occur in tunicates while those for neural crest, adenohypophysis and trigeminal placode and ganglion are in vertebrates; however, a minor peak for the adenohypophysis occurs with the chordates [53].…”

“…For example, an analysis of genes involved in development of sensory structures in vertebrates showed that genes for the eyes, including the lens evolved first, with peaks for the number of new genes for the retina and eye evolving in deuterostomes and for the lens in cephalochordates [53]. By contrast, the peak appearances of new genes for the olfactory system, ear and lateral line as well as that for cranial placodes occur in tunicates while those for neural crest, adenohypophysis and trigeminal placode and ganglion are in vertebrates; however, a minor peak for the adenohypophysis occurs with the chordates [53]. When this type of analysis was applied to the brain regions, genes for the whole brain, forebrain (including diencephalon and telencephalon), midbrain and hindbrain made their peak appearance in amphioxus, although there were minor peaks for all but the midbrain genes at the base of the metazoan and in the vertebrates (figure 3) [1].…”

Evolutionary hallmarks of the human proteome: chasing the age and coregulation of protein-coding genes

“…is an important piece of information that can be inferred in different ways and has been used in some genome-scale studies and in some studies on gene families [9]. Phylostratigraphy is the usual methodology applied to find the origin and emergence of genes [10, 11]. Previous phylogenetic studies showed that the evolutionary history of different coding parts of the genome have relations with diseases [12], codon usage [13], essentiality, interactions [14], stemness and self-renewal [15].…”

The characterization of larval homology: transcriptomic insights into the origin and evolution of animal life cycles

“…While these analyses are widely used in the literature (e.g. Domazet-Lošo et al 2007, Domazet-Lošo and Tautz 2010, Sestak et al 2013, Neme and Tautz 2013, Maxwell et al 2014, certain studies have questioned the reliability of phylostratigraphy (Zhang and Moyers 2014).…”

“…Therefore, in response to the proliferation of bioinformatic techniques using gene age (Domazet-Lošo et al 2007, Domazet-Lošo and Tautz 2010, Sestak et al 2013, I have taken a transcriptomic approach to inform existing hypotheses for life cycle evolution. I predict that each evolutionary hypothesis will present different signatures in the activity of the genome in larvae, juveniles, and adults of extant biphasic species.…”