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12. The origin and phylogeny of Margaritiferidae (Bivalvia, Unionoida): a synthesis of molecular and fossil data

Author

Ministerio de Economía y Competitividad (España), Araujo, Rafael, Schneider, Simon, Roe, Kevin J., Erpenbeck, Dirk, Machordom, Annie, Ministerio de Economía y Competitividad (España), Araujo, Rafael, Schneider, Simon, Roe, Kevin J., Erpenbeck, Dirk, and Machordom, Annie

Abstract

The family Margaritiferidae is a small but widely distributed group within the Unionoida, or freshwater mussels, whose taxonomy and systematics has been the subject of numerous publications. Despite several efforts, there is no consensus on which characters reliably diagnose this family. Herein, we present the results of a phylogenetic analysis of the most comprehensive data set for Margaritiferidae in terms of taxa and phylogenetic markers assembled to date, including eleven out of the twelve margaritiferid species currently considered valid. In addition, we review the fossil record of the family and attempt to integrate fossil and DNA sequence data to provide a diagnosis of Margaritiferidae, identify its origin and biogeographic patterns, and determine the systematic relationships of its constituent species and their taxonomic affinities. We assembled a molecular data set comprised of five markers: COI, 16S, 28S, 18S and histone 3 for a total of 59 specimens representing eleven species of Margaritifera. Our results indicate that the family Margaritiferidae is a monophyletic group comprised of the single genus Margaritifera, which includes the following 12 species: M. dahurica, M. margaritifera, M. monodonta, M. middendorffi, M. laevis, M. marrianae, M. hembeli, M. falcata, M. laosensis, M. auricularia and M. marocana plus the unstudied M. homsensis. Estimates of divergence times using fossil calibrations or mean substitution rates produced dramatically different results. Divergence estimates based on the fossil calibrations were 10 times higher than those obtained applying the mean substitution rates. The current distribution of the family implies dispersal across marine or brackish waters by their host fish, leaving a fossil record on four continents that dates to the Mesozoic. Margaritiferidae appear to be derived from putative ancestor in the Silesunionidae, with a likely origin in Asia. We suggest that Margaritiferidae had spread along the Tethys margins and c

Published
2017

15. Permanent Genetic Resources added to Molecular Ecology Resources Database 1 May 2009-31 July 2009

Author

Almany, Glenn R., DE Arruda, Maurício P., Arthofer, Wolfgang, Atallah, Z.K., Beissinger, Steven R., Berumen, Michael L., Bogdanowicz, S M, Brown, S D, Bruford, Michael W, Burdine, C, Busch, Jeremiah W, Campbell, Nathan R, Carey, D, Carstens, Bryan C, Chu, K H, Cubeta, Marc A, Cuda, J P, Cui, Zhaoxia, Datnoff, L E, Dávila, J A, Davis, Emily S, Davis, R M, Diekmann, Onno E, Eizirik, Eduardo, Fargallo, J A, Fernandes, Fabiano, Fukuda, Hideo, Gale, L R, Gallagher, Elizabeth, Gao, Yongqiang, Girard, Philippe, Godhe, Anna, Gonçalves, Evonnildo C, Gouveia, Licinia, Grajczyk, Amber M, Grose, M J, Gu, Zhifeng, Halldén, Christer, Härnström, Karolina, Hemmingsen, Amanda H, Holmes, Gerald, Huang, C H, Huang, Chuan-Chin, Hudman, S P, Jones, Geoffrey P, Kanetis, Loukas, Karunasagar, Iddya, Karunasagar, Indrani, Keyghobadi, Nusha, Klosterman, S J, Klug, Page E, Koch, J, Koopman, Margaret M, Köppler, Kirsten, Koshimizu, Eriko, Krumböck, Susanne, Kubisiak, T, Landis, J B, Lasta, Mario L, Lee, Chow-Yang, Li, Qianqian, Li, Shou-Hsien, Lin, Rong-Chien, Liu, M, Liu, Na, Liu, W C, Liu, Yuan, Loiseau, A, Luan, Weisha, Maruthachalam, K K, McCormick, Helen M, Mellick, Rohan, Monnahan, P J, Morielle-Versute, Eliana, Murray, Tomás E, Narum, Shawn R, Neufeld, Katie, De Nova, P J G, Ojiambo, Peter S, Okamoto, Nobuaki, Othman, Ahmad Sofiman, Overholt, W A, Pardini, Renata, Paterson, Ian G, Patty, Olivia A, Paxton, Robert J, Planes, Serge, Porter, Carolyn, Pratchett, Morgan S, Püttker, Thomas, Rasic, Gordana, Rasool, Bilal, Rey, O, Riegler, Markus, Riehl, C, Roberts, John M K, Roberts, P D, Rochel, Elisabeth, Roe, Kevin J, Rossetto, Maurizio, Ruzzante, Daniel E, Sakamoto, Takashi, Saravanan, V, Sarturi, Cladinara Roberts, Schmidt, Anke, Schneider, Maria Paula Cruz, Schuler, Hannes, Serb, Jeanne M, Serrão, Ester T A, Shi, Yaohua, Silva, Artur, Sin, Y W, Sommer, Simone, Stauffer, Christian, Strüssmann, Carlos Augusto, Subbarao, K V, Syms, Craig, Tan, Feng, Tejedor, Eugenio Daniel, Thorrold, Simon R, Trigiano, Robert N, Trucco, María I, Tsuchiya-Jerep, Mirian Tieko Nunes, Vergara, P, Van De Vliet, Mirjam S, Wadl, Phillip A, Wang, Aimin, Wang, Hongxia, Wang, R X, Wang, Xinwang, Wang, Yan, Weeks, Andrew R, Wei, Fuwen, Werner, William J, Wiley, E O, Williams, D A, Wilkins, Richard J, Wisely, Samantha M, With, Kimberly A, Wu, Danhua, Yao, Cheng-Te, Yau, Cynthia, Yeap, Beng-Keok, Zhai, Bao-Ping, Zhan, Xiangjiang, Zhang, Guo-Yan, Zhang, S Y, Zhao, Ru, Zhu, Lifeng, Almany, Glenn R., DE Arruda, Maurício P., Arthofer, Wolfgang, Atallah, Z.K., Beissinger, Steven R., Berumen, Michael L., Bogdanowicz, S M, Brown, S D, Bruford, Michael W, Burdine, C, Busch, Jeremiah W, Campbell, Nathan R, Carey, D, Carstens, Bryan C, Chu, K H, Cubeta, Marc A, Cuda, J P, Cui, Zhaoxia, Datnoff, L E, Dávila, J A, Davis, Emily S, Davis, R M, Diekmann, Onno E, Eizirik, Eduardo, Fargallo, J A, Fernandes, Fabiano, Fukuda, Hideo, Gale, L R, Gallagher, Elizabeth, Gao, Yongqiang, Girard, Philippe, Godhe, Anna, Gonçalves, Evonnildo C, Gouveia, Licinia, Grajczyk, Amber M, Grose, M J, Gu, Zhifeng, Halldén, Christer, Härnström, Karolina, Hemmingsen, Amanda H, Holmes, Gerald, Huang, C H, Huang, Chuan-Chin, Hudman, S P, Jones, Geoffrey P, Kanetis, Loukas, Karunasagar, Iddya, Karunasagar, Indrani, Keyghobadi, Nusha, Klosterman, S J, Klug, Page E, Koch, J, Koopman, Margaret M, Köppler, Kirsten, Koshimizu, Eriko, Krumböck, Susanne, Kubisiak, T, Landis, J B, Lasta, Mario L, Lee, Chow-Yang, Li, Qianqian, Li, Shou-Hsien, Lin, Rong-Chien, Liu, M, Liu, Na, Liu, W C, Liu, Yuan, Loiseau, A, Luan, Weisha, Maruthachalam, K K, McCormick, Helen M, Mellick, Rohan, Monnahan, P J, Morielle-Versute, Eliana, Murray, Tomás E, Narum, Shawn R, Neufeld, Katie, De Nova, P J G, Ojiambo, Peter S, Okamoto, Nobuaki, Othman, Ahmad Sofiman, Overholt, W A, Pardini, Renata, Paterson, Ian G, Patty, Olivia A, Paxton, Robert J, Planes, Serge, Porter, Carolyn, Pratchett, Morgan S, Püttker, Thomas, Rasic, Gordana, Rasool, Bilal, Rey, O, Riegler, Markus, Riehl, C, Roberts, John M K, Roberts, P D, Rochel, Elisabeth, Roe, Kevin J, Rossetto, Maurizio, Ruzzante, Daniel E, Sakamoto, Takashi, Saravanan, V, Sarturi, Cladinara Roberts, Schmidt, Anke, Schneider, Maria Paula Cruz, Schuler, Hannes, Serb, Jeanne M, Serrão, Ester T A, Shi, Yaohua, Silva, Artur, Sin, Y W, Sommer, Simone, Stauffer, Christian, Strüssmann, Carlos Augusto, Subbarao, K V, Syms, Craig, Tan, Feng, Tejedor, Eugenio Daniel, Thorrold, Simon R, Trigiano, Robert N, Trucco, María I, Tsuchiya-Jerep, Mirian Tieko Nunes, Vergara, P, Van De Vliet, Mirjam S, Wadl, Phillip A, Wang, Aimin, Wang, Hongxia, Wang, R X, Wang, Xinwang, Wang, Yan, Weeks, Andrew R, Wei, Fuwen, Werner, William J, Wiley, E O, Williams, D A, Wilkins, Richard J, Wisely, Samantha M, With, Kimberly A, Wu, Danhua, Yao, Cheng-Te, Yau, Cynthia, Yeap, Beng-Keok, Zhai, Bao-Ping, Zhan, Xiangjiang, Zhang, Guo-Yan, Zhang, S Y, Zhao, Ru, and Zhu, Lifeng

Abstract

This article documents the addition of 512 microsatellite marker loci and nine pairs of Single Nucleotide Polymorphism (SNP) sequencing primers to the Molecular Ecology Resources Database. Loci were developed for the following species: Alcippe morrisonia morrisonia, Bashania fangiana, Bashania fargesii, Chaetodon vagabundus, Colletes floralis, Coluber constrictor flaviventris, Coptotermes gestroi, Crotophaga major, Cyprinella lutrensis, Danaus plexippus, Fagus grandifolia, Falco tinnunculus, Fletcherimyia fletcheri, Hydrilla verticillata, Laterallus jamaicensis coturniculus, Leavenworthia alabamica, Marmosops incanus, Miichthys miiuy, Nasua nasua, Noturus exilis, Odontesthes bonariensis, Quadrula fragosa, Pinctada maxima, Pseudaletia separata, Pseudoperonospora cubensis, Podocarpus elatus, Portunus trituberculatus, Rhagoletis cerasi, Rhinella schneideri, Sarracenia alata, Skeletonema marinoi, Sminthurus viridis, Syngnathus abaster, Uroteuthis (Photololigo) chinensis, Verticillium dahliae, Wasmannia auropunctata, and Zygochlamys patagonica. These loci were cross-tested on the following species: Chaetodon baronessa, Falco columbarius, Falco eleonorae, Falco naumanni, Falco peregrinus, Falco subbuteo, Didelphis aurita, Gracilinanus microtarsus, Marmosops paulensis, Monodelphis Americana, Odontesthes hatcheri, Podocarpus grayi, Podocarpus lawrencei, Podocarpus smithii, Portunus pelagicus, Syngnathus acus, Syngnathus typhle,Uroteuthis (Photololigo) edulis, Uroteuthis (Photololigo) duvauceli and Verticillium albo-atrum. This article also documents the addition of nine sequencing primer pairs and sixteen allele specific primers or probes for Oncorhynchus mykiss and Oncorhynchus tshawytscha; these primers and assays were cross-tested in both species.

Published
2009
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16. Incongruence between mt DNA and nuclear data in the freshwater mussel genus Cyprogenia ( Bivalvia: Unionidae) and its impact on species delineation.

Author

Chong, Jer Pin, Harris, John L., and Roe, Kevin J.

Subjects
MITOCHONDRIAL DNA, BIVALVES, FRESHWATER mussels
Abstract

Accurately identifying species is a crucial step for developing conservation strategies for freshwater mussels, one of the most imperiled faunas in North America. This study uses genetic data to re-examine species delineation in the genus Cyprogenia. Historically, Cyprogenia found west of the Mississippi River have been ascribed to Cyprogenia aberti (Conrad ), and those east of the Mississippi River were classified as Cyprogenia stegaria (Rafinesque 1820). Previous studies using mitochondrial DNA sequences indicated that C. aberti and C. stegaria were not reciprocally monophyletic groups, suggesting the need for systematic revision. We generated a novel dataset consisting of 10 microsatellite loci and combined it with sequence data from the mitochondrial ND1 gene for 223 Cyprogenia specimens. Bayesian analysis of the ND1 nucleotide sequences identified two divergent clades that differ by 15.9%. Members of these two clades occur sympatrically across most sampling locations. In contrast, microsatellite genotypes support recognition of three allopatric clusters defined by major hydrologic basins. The divergent mitochondrial lineages are highly correlated with the color of the conglutinate lures used by mussels to attract and infest host fishes, and tests for selection at the ND1 locus were positive. We infer that the incongruence between mt DNA and microsatellite data in Cyprogenia may be the result of a combination of incomplete lineage sorting and balancing selection on lure color. Our results provide further evidence that mitochondrial markers are not always neutral with respect to selection, and highlight the potential problems of relying on a single-locus-marker for delineating species. [ABSTRACT FROM AUTHOR]

Published
2016
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17. Incongruence between mtDNA and nuclear data in the freshwater mussel genus Cyprogenia (Bivalvia: Unionidae) and its impact on species delineation.

Author

Chong JP, Harris JL, and Roe KJ

Abstract

Accurately identifying species is a crucial step for developing conservation strategies for freshwater mussels, one of the most imperiled faunas in North America. This study uses genetic data to re-examine species delineation in the genus Cyprogenia. Historically, Cyprogenia found west of the Mississippi River have been ascribed to Cyprogenia aberti (Conrad 1850), and those east of the Mississippi River were classified as Cyprogenia stegaria (Rafinesque 1820). Previous studies using mitochondrial DNA sequences indicated that C. aberti and C. stegaria were not reciprocally monophyletic groups, suggesting the need for systematic revision. We generated a novel dataset consisting of 10 microsatellite loci and combined it with sequence data from the mitochondrial ND1 gene for 223 Cyprogenia specimens. Bayesian analysis of the ND1 nucleotide sequences identified two divergent clades that differ by 15.9%. Members of these two clades occur sympatrically across most sampling locations. In contrast, microsatellite genotypes support recognition of three allopatric clusters defined by major hydrologic basins. The divergent mitochondrial lineages are highly correlated with the color of the conglutinate lures used by mussels to attract and infest host fishes, and tests for selection at the ND1 locus were positive. We infer that the incongruence between mtDNA and microsatellite data in Cyprogenia may be the result of a combination of incomplete lineage sorting and balancing selection on lure color. Our results provide further evidence that mitochondrial markers are not always neutral with respect to selection, and highlight the potential problems of relying on a single-locus-marker for delineating species.

Published
2016
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