title: Molecular Evidence for Convergence and Parallelism in Evolution of Complex Brains of Cephalopod Molluscs: Insights from Visual Systems.
abstract: Coleoid cephalopods show remarkable evolutionary convergence with vertebrates in their neural organization, including (1) eyes and visual system with optic lobes, (2) specialized parts of the brain controlling learning and memory, such as vertical lobes, and (3) unique vasculature supporting such complexity of the central nervous system. We performed deep sequencing of eye transcriptomes of pygmy squids (Idiosepius paradoxus) and chambered nautiluses (Nautilus pompilius) to decipher the molecular basis of convergent evolution in cephalopods. RNA-seq was complemented by in situ hybridization to localize the expression of selected genes. We found three types of genomic innovations in the evolution of complex brains: (1) recruitment of novel genes into morphogenetic pathways, (2) recombination of various coding and regulatory regions of different genes, often called "evolutionary tinkering" or "co-option", and (3) duplication and divergence of genes. Massive recruitment of novel genes occurred in the evolution of the "camera" eye from nautilus' "pinhole" eye. We also showed that the type-2 co-option of transcription factors played important roles in the evolution of the lens and visual neurons. In summary, the cephalopod convergent morphological evolution of the camera eyes was driven by a mosaic of all types of gene recruitments. In addition, our analysis revealed unexpected variations of squids' opsins, retinochromes, and arrestins, providing more detailed information, valuable for further research on intra-ocular and extra-ocular photoreception of the cephalopods.
authors.affiliation: *Research Fellow of the Japan Society for the Promotion of Science; Center for Information Biology, National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 411-8540, Japan; Center for Information Biology, National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 411-8540, Japan;
authors.forename: M A
authors.initials: MA
authors.lastname: Yoshida
authors.affiliation: Department of Computer Bioscience, Nagahama Institute of Bio-science and Technology, 1266 Tamura, Nagahama, Shiga 526-0829 Japan;
authors.forename: A
authors.initials: A
authors.lastname: Ogura
authors.affiliation: Center for Information Biology, National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 411-8540, Japan;
authors.forename: K
authors.initials: K
authors.lastname: Ikeo
authors.affiliation: Department for Marine Biodiversity Research, Japan Agency for Marine-Earth Science and Technology, 2-15, Natsushima, Yokosuka, Kanagawa 237-0061, Japan;
authors.forename: S
authors.initials: S
authors.lastname: Shigeno
authors.affiliation: Toba Aquarium, 3-3-6 Toba, Toba, Mie 517-8517, Japan;
authors.forename: T
authors.initials: T
authors.lastname: Moritaki
authors.affiliation: The Whitney Laboratory for Marine Bioscience, University of Florida, 9505 Ocean Shore Blvd, St Augustine, FL 32080, USA; Department of Neuroscience, University of Florida, Gainesville, FL 32611, USA;
authors.forename: G C
authors.initials: GC
authors.lastname: Winters
authors.affiliation: The Whitney Laboratory for Marine Bioscience, University of Florida, 9505 Ocean Shore Blvd, St Augustine, FL 32080, USA;
authors.forename: A B
authors.initials: AB
authors.lastname: Kohn
authors.affiliation: The Whitney Laboratory for Marine Bioscience, University of Florida, 9505 Ocean Shore Blvd, St Augustine, FL 32080, USA; Department of Neuroscience, University of Florida, Gainesville, FL 32611, USA; **McKnight Brain Institute, University of Florida, Gainesville, FL 32611, USA moroz@whitney.ufl.edu.
authors.forename: L L
authors.initials: LL
authors.lastname: Moroz
mesh_terms: D000595:Amino Acid Sequence; D000818:Animals; D019393:Arrestin / Q000235:genetics / Q000378:metabolism; D001921:Brain / Q000033:anatomy & histology*; D049830:Cephalopoda / Q000033:anatomy & histology* / Q000235:genetics; D019143:Evolution, Molecular; D018507:Gene Expression Regulation, Developmental / Q000502:physiology*; D007908:Lens, Crystalline; D009799:Ocular Physiological Phenomena / Q000235:genetics*; D010786:Photoreceptor Cells / Q000502:physiology; D010802:Phylogeny; D020033:Protein Isoforms
chemical_list: D019393:Arrestin; D020033:Protein Isoforms