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      Divergence of the Venom Exogene Repertoire in Two Sister Species of Turriconus

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          Abstract

          The genus Conus comprises approximately 700 species of venomous marine cone snails that are highly efficient predators of worms, snails, and fish. In evolutionary terms, cone snails are relatively young with the earliest fossil records occurring in the Lower Eocene, 55 Ma. The rapid radiation of cone snail species has been accompanied by remarkably high rates of toxin diversification. To shed light on the molecular mechanisms that accompany speciation, we investigated the toxin repertoire of two sister species, Conus andremenezi and Conus praecellens, that were until recently considered a single variable species. A total of 196 and 250 toxin sequences were identified in the venom gland transcriptomes of C. andremenezi and C. praecellens belonging to 25 and 29 putative toxin gene superfamilies, respectively. Comparative analysis with closely ( Conus tribblei and Conus lenavati) and more distantly related species ( Conus geographus) suggests that speciation is associated with significant diversification of individual toxin genes (exogenes) whereas the expression pattern of toxin gene superfamilies within lineages remains largely conserved. Thus, changes within individual toxin sequences can serve as a sensitive indicator for recent speciation whereas changes in the expression pattern of gene superfamilies are likely to reflect more dramatic differences in a species’ interaction with its prey, predators, and competitors.

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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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            Double indexing overcomes inaccuracies in multiplex sequencing on the Illumina platform

            Due to the increasing throughput of current DNA sequencing instruments, sample multiplexing is necessary for making economical use of available sequencing capacities. A widely used multiplexing strategy for the Illumina Genome Analyzer utilizes sample-specific indexes, which are embedded in one of the library adapters. However, this and similar multiplex approaches come with a risk of sample misidentification. By introducing indexes into both library adapters (double indexing), we have developed a method that reveals the rate of sample misidentification within current multiplex sequencing experiments. With ~0.3% these rates are orders of magnitude higher than expected and may severely confound applications in cancer genomics and other fields requiring accurate detection of rare variants. We identified the occurrence of mixed clusters on the flow as the predominant source of error. The accuracy of sample identification is further impaired if indexed oligonucleotides are cross-contaminated or if indexed libraries are amplified in bulk. Double-indexing eliminates these problems and increases both the scope and accuracy of multiplex sequencing on the Illumina platform.
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              Extensive and continuous duplication facilitates rapid evolution and diversification of gene families.

              The origin of novel gene functions through gene duplication, mutation, and natural selection represents one of the mechanisms by which organisms diversify and one of the possible paths leading to adaptation. Nonetheless, the extent, role, and consequences of duplications in the origins of ecological adaptations, especially in the context of species interactions, remain unclear. To explore the evolution of a gene family that is likely linked to species associations, we investigated the evolutionary history of the A-superfamily of conotoxin genes of predatory marine cone snails (Conus species). Members of this gene family are expressed in the venoms of Conus species and are presumably involved in predator-prey associations because of their utility in prey capture. We recovered sequences of this gene family from genomic DNA of four closely related species of Conus and reconstructed the evolutionary history of these genes. Our study is the first to directly recover conotoxin genes from Conus genomes to investigate the evolution of conotoxin gene families. Our results revealed a phenomenon of rapid and continuous gene turnover that is coupled with heightened rates of evolution. This continuous duplication pattern has not been observed previously, and the rate of gene turnover is at least two times higher than estimates from other multigene families. Conotoxin genes are among the most rapidly evolving protein-coding genes in metazoans, a phenomenon that may be facilitated by extensive gene duplications and have driven changes in conotoxin functions through neofunctionalization. Together these mechanisms led to dramatically divergent arrangements of A-superfamily conotoxin genes among closely related species of Conus. Our findings suggest that extensive and continuous gene duplication facilitates rapid evolution and drastic divergence in venom compositions among species, processes that may be associated with evolutionary responses to predator-prey interactions.
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                Author and article information

                Journal
                Genome Biol Evol
                Genome Biol Evol
                gbe
                Genome Biology and Evolution
                Oxford University Press
                1759-6653
                September 2017
                23 August 2017
                23 August 2017
                : 9
                : 9
                : 2211-2225
                Affiliations
                [1 ]Eccles Institute of Human Genetics, University of Utah
                [2 ]Marine Science Institute, University of the Philippines-Diliman, Quezon City, Philippines
                [3 ]Institute für Populationsgenetik, Vetmeduni, Vienna, 1210, Austria
                [4 ]School of Life Sciences and Technology, Tongji University, Shanghai, China
                [5 ]A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Science, Moscow, Russia
                [6 ]Department of Biology, University of Utah
                [7 ]Philippine Genome Center, University of the Philippines, Quezon City, Philippines
                [8 ]USTAR Center for Genetic Discovery, University of Utah
                Author notes

                Associate editor: Mandë Holford

                Data deposition: This project has been deposited at GenBank under the accessions MF576542 - MF576988

                [* ]Corresponding author: E-mail: helena.safavi@ 123456utah.edu .
                Article
                evx157
                10.1093/gbe/evx157
                5604253
                28922871
                6086300d-3b02-45e2-80eb-ddae8ed46f38
                © The Author 2017. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com

                History
                : 22 August 2017
                Page count
                Pages: 15
                Funding
                Funded by: National Institutes of Health 10.13039/100000002
                Award ID: GM 48677
                Award ID: GM 099939
                Funded by: National Natural Science Foundation of China 10.13039/501100001809
                Award ID: 31500626
                Categories
                Research Article

                Genetics
                venom evolution,speciation,conotoxins,exogenes
                Genetics
                venom evolution, speciation, conotoxins, exogenes

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