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      The octopus genome and the evolution of cephalopod neural and morphological novelties

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          Abstract

          Coleoid cephalopods (octopus, squid, and cuttlefish) are active, resourceful predators with a rich behavioral repertoire 1 . They have the largest nervous systems among the invertebrates 2 and present other striking morphological innovations including camera-like eyes, prehensile arms, a highly derived early embryogenesis, and the most sophisticated adaptive coloration system among all animals 1, 3 . To investigate the molecular bases of cephalopod brain and body innovations we sequenced the genome and multiple transcriptomes of the California two-spot octopus, Octopus bimaculoides. We found no evidence for hypothesized whole genome duplications in the octopus lineage 46 . The core developmental and neuronal gene repertoire of the octopus is broadly similar to that found across invertebrate bilaterians, except for massive expansions in two gene families formerly thought to be uniquely enlarged in vertebrates: the protocadherins, which regulate neuronal development, and the C2H2 superfamily of zinc finger transcription factors. Extensive mRNA editing generates transcript and protein diversity in genes involved in neural excitability, as previously described 7 , as well as in genes participating in a broad range of other cellular functions. We identified hundreds of cephalopod-specific genes, many of which showed elevated expression levels in such specialized structures as the skin, the suckers, and the nervous system. Finally, we found evidence for large-scale genomic rearrangements that are closely associated with transposable element expansions. Our analysis suggests that substantial expansion of a handful of gene families, along with extensive remodeling of genome linkage and repetitive content, played a critical role in the evolution of cephalopod morphological innovations, including their large and complex nervous systems.

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          Most cited references40

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          MRBAYES: Bayesian inference of phylogenetic trees.

          The program MRBAYES performs Bayesian inference of phylogeny using a variant of Markov chain Monte Carlo. MRBAYES, including the source code, documentation, sample data files, and an executable, is available at http://brahms.biology.rochester.edu/software.html.
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            Is Open Access

            The amphioxus genome and the evolution of the chordate karyotype.

            Lancelets ('amphioxus') are the modern survivors of an ancient chordate lineage, with a fossil record dating back to the Cambrian period. Here we describe the structure and gene content of the highly polymorphic approximately 520-megabase genome of the Florida lancelet Branchiostoma floridae, and analyse it in the context of chordate evolution. Whole-genome comparisons illuminate the murky relationships among the three chordate groups (tunicates, lancelets and vertebrates), and allow not only reconstruction of the gene complement of the last common chordate ancestor but also partial reconstruction of its genomic organization, as well as a description of two genome-wide duplications and subsequent reorganizations in the vertebrate lineage. These genome-scale events shaped the vertebrate genome and provided additional genetic variation for exploitation during vertebrate evolution.
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              Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models.

              Q. Z. Yang (2000)
              Approximate methods for estimating the numbers of synonymous and nonsynonymous substitutions between two DNA sequences involve three steps: counting of synonymous and nonsynonymous sites in the two sequences, counting of synonymous and nonsynonymous differences between the two sequences, and correcting for multiple substitutions at the same site. We examine complexities involved in those steps and propose a new approximate method that takes into account two major features of DNA sequence evolution: transition/transversion rate bias and base/codon frequency bias. We compare the new method with maximum likelihood, as well as several other approximate methods, by examining infinitely long sequences, performing computer simulations, and analyzing a real data set. The results suggest that when there are transition/transversion rate biases and base/codon frequency biases, previously described approximate methods for estimating the nonsynonymous/synonymous rate ratio may involve serious biases, and the bias can be both positive and negative. The new method is, in general, superior to earlier approximate methods and may be useful for analyzing large data sets, although maximum likelihood appears to always be the method of choice.
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                Author and article information

                Journal
                0410462
                6011
                Nature
                Nature
                Nature
                0028-0836
                1476-4687
                27 February 2016
                13 August 2015
                17 March 2016
                : 524
                : 7564
                : 220-224
                Affiliations
                [1 ]Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637, USA
                [2 ]Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa 9040495, Japan
                [3 ]Centre for Organismal Studies, University of Heidelberg, Grabengasse 1, 69117 Heidelberg, Germany
                [4 ]Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720, USA
                [5 ]Department of Neurobiology, University of Chicago, Chicago, IL 60637, USA
                [6 ]Department of Energy Joint Genome Institute, Walnut Creek, CA 94598, USA
                Author notes
                [+ ]Correspondence and requests for materials should be addressed to C.W.R. ( cragsdale@ 123456uchicago.edu ) or D.S.R. ( dsrokhsar@ 123456gmail.com )
                [*]

                contributed equally

                Article
                NIHMS701285
                10.1038/nature14668
                4795812
                26268193
                90036826-f1cf-48f5-aaa7-6cad1b4269d5

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