Abstract
In Bilateria, Pax6, Six, Eya and Dach families of transcription factors underlie the development and evolution of morphologically and phyletically distinct eyes, including the compound eyes in Drosophila and the camera-type eyes in vertebrates, indicating that bilaterian eyes evolved under the strong influence of ancestral developmental gene regulation. However the conservation in eye developmental genetics deeper in the Eumetazoa, and the origin of the conserved gene regulatory apparatus controlling eye development remain unclear due to limited comparative developmental data from Cnidaria. Here we show in the eye-bearing scyphozoan cnidarian Aurelia that the ectodermal photosensory domain of the developing medusa sensory structure known as the rhopalium expresses sine oculis (so)/six1/2 and eyes absent/eya, but not optix/six3/6 or pax (A&B). In addition, the so and eya co-expression domain encompasses the region of active cell proliferation, neurogenesis, and mechanoreceptor development in rhopalia. Consistent with the role of so and eya in rhopalial development, developmental transcriptome data across Aurelia life cycle stages show upregulation of so and eya, but not optix or pax (A&B), during medusa formation. Moreover, pax6 and dach are absent in the Aurelia genome, and thus are not required for eye development in Aurelia. Our data are consistent with so and eya, but not optix, pax or dach, having conserved functions in sensory structure specification across Eumetazoa. The lability of developmental components including Pax genes relative to so-eya is consistent with a model of sense organ development and evolution that involved the lineage specific modification of a combinatorial code that specifies animal sense organs.
Highlights
Eye evolution has fascinated biologists since Darwin
We show in the eye-bearing scyphozoan cnidarian Aurelia that the ectodermal photosensory domain of the developing medusa sensory structure known as the rhopalium expresses sine oculis/ six1/2 and eyes absent/eya, but not optix/six3/6 or pax (A&B)
We explore the role of this suite of developmental genes in Aurelia eye development as a step in generating a more complete understanding of the role of these genes in eye development in the Cnidaria, the sister taxon to the well-studied Bilatera [5, 6]
Summary
Eye evolution has fascinated biologists since Darwin He [1] considered an eye one of “the organs of extreme perfection and complication” that appeared “absurd in the highest possible degree” to have resulted from natural selection. Developmental genetics provided a surprise; vertebrate eyes and insect eyes, previously thought to have arisen independently, develop via a conserved gene regulatory network, the so-called “retinal determination gene network (RDGN)”, consisting of homologous transcription factors, Pax, Six, Eya and Dach (named twin of eyeless/eyeless, sine oculis (so)/optix, eyes absent and dachshund (dac), respectively, in insects; reviewed in [3]) This suggested deep homology of eye development across the Bilateria. We explore the role of this suite of developmental genes in Aurelia eye development as a step in generating a more complete understanding of the role of these genes in eye development in the Cnidaria, the sister taxon to the well-studied Bilatera [5, 6]
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