Loss of the six3/6 controlling pathways might have resulted in pinhole-eye evolution in Nautilus

Abstract

Coleoid cephalopods have an elaborate camera eye whereas nautiloids have primitive pinhole eye without lens and cornea. The Nautilus pinhole eye provides a unique example to explore the module of lens formation and its evolutionary mechanism. Here, we conducted an RNA-seq study of developing eyes of Nautilus and pygmy squid. First, we found that evolutionary distances from the common ancestor to Nautilus or squid are almost the same. Although most upstream eye development controlling genes were expressed in both species, six3/6 that are required for lens formation in vertebrates was not expressed in Nautilus. Furthermore, many downstream target genes of six3/6 including crystallin genes and other lens protein related genes were not expressed in Nautilus. As six3/6 and its controlling pathways are widely conserved among molluscs other than Nautilus, the present data suggest that deregulation of the six3/6 pathway led to the pinhole eye evolution in Nautilus.

Transcriptome Analysis of Nautilus and Pygmy Squid Developing Eye Provides Insights in Lens and Eye Evolution

“…These data correspond to developing eyes from Idiosepius paradoxus (pygmy squid) embryos at stage 24 and Nautilus pompilius embryos 30 days in development [5]. …”

“…Raw sequencing reads were obtained from the DNA Data Bank of Japan (DDBJ; ID:DRA000453)[5]. These data correspond to developing eyes from Idiosepius paradoxus (pygmy squid) embryos at stage 24 and Nautilus pompilius embryos 30 days in development [5].…”

“…Recently the transcriptome of both species has been established and assembled de novo [5]. In the present paper this information is analyzed thoroughly to compare gene expression in hope that it will provide insights into the evolution of eye elements in invertebrates and vertebrates.…”

Ancestry, Origin and Early Evolution of Ammonoids

“…Extant Nautilida have pinhole eyes which could well represent the plesiomorphic condition for cephalopods as the outgroup has less complex photoreceptor organs. However, the pinhole camera eye (as suggested by a novel molecular study : Ogura et al 2013) might be a specialization of the Nautilida just like the great number of arms (Shigeno et al 2008Sasaki et al 2010). Ammonoids are stem coleoids and are thus situated on a lineage that evolved camera type eyes.…”

“…Indeed, not many features (pinhole eye, 90 arms, large embryonic shell, hood etc.) appear to have developed specifically in the lineage leading up to extant Nautilus (Shigeno et al 2008Sasaki et al 2010;Ogura et al 2013), potentially all after their separation from the Orthocerida . Coleoids, which are more closely related to ammonoids, are not necessarily a better model for ammonoid anatomy considering their evolution since their separation over 400 Ma ago .…”