Abstract
Coleoid cephalopods like squids have a camera-type eye similar to vertebrates. On the other hand, Nautilus (Nautiloids) has a pinhole eye that lacks lens and cornea. Since pygmy squid and Nautilus are closely related species they are excellent model organisms to study eye evolution. Having being able to collect Nautilus embryos, we employed next-generation RNA sequencing using Nautilus and pygmy squid developing eyes. Their transcriptomes were compared and analyzed. Enrichment analysis of Gene Ontology revealed that contigs related to nucleic acid binding were largely up-regulated in squid, while the ones related to metabolic processes and extracellular matrix-related genes were up-regulated in Nautilus. These differences are most likely correlated with the complexity of tissue organization in these species. Moreover, when the analysis focused on the eye-related contigs several interesting patterns emerged. First, contigs from both species related to eye tissue differentiation and morphogenesis as well as to cilia showed best hits with their Human counterparts, while contigs related to rabdomeric photoreceptors showed the best hit with their Drosophila counterparts. This bolsters the idea that eye morphogenesis genes have been generally conserved in evolution, and compliments other studies showing that genes involved in photoreceptor differentiation clearly follow the diversification of invertebrate (rabdomeric) and vertebrate (ciliated) photoreceptors. Interestingly some contigs showed as good a hit with Drosophila and Human homologues in Nautilus and squid samples. One of them, capt/CAP1, is known to be preferentially expressed in Drosophila developing eye and in vertebrate lens. Importantly our analysis also provided evidence of gene duplication and diversification of their function in both species. One of these genes is the Neurofibromatosis 1 (NF1/Nf1), which in mice has been implicated in lens formation, suggesting a hitherto unsuspected role in the evolution of the lens in molluscs.
Highlights
The eye has been one of the wonders of evolution
Have all eyes evolved from a prototype eye or have they been evolved independently many times? The ideas on the monophyletic origin of eyes have been bolstered by regulation of their morphogenesis by pax-6, heralded as the eye master gene in all species [1]
Vertebrates have ciliary photoreceptors with disks stacked together and are embedded in the retina away from the direct light [2]. This is an important difference, which might infer independent evolution of photoreceptors, even though such more complex scenario is compatible with pax-6 expression
Summary
The eye has been one of the wonders of evolution. That the common ancestor of all eyes must have been a cell (or few cells) that responded to light is more or less an accepted notion. Human and Drosophila fasta files were compared using the BLAST tool[10] to the Nautilus and squid transcriptomes making the raw eyerelated contigs for each of the organism.
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