Molecular phylogeny of the Indochinese freshwater mussel genus Scabies Haas, 1911 (Bivalvia: Unionidae)
Keywords:
Indochina, freshwater mussels, Radiatula, taxonomy, UnionidaeAbstract
Molecular phylogeny of the Indochinese freshwater mussel genus Scabies Haas, 1911 was studied. The examined taxa included all seven recognized species of the genus Scabies (S. phaselus, S. anceps, S. scobinatus, S. crispata, S. mandarinus, S. nucleus and S. songkramensis) and two closely related Indochinese species currently assigned to the genus Radiatula Simpson, 1900 (R. humilis and R. pilata). Maximum likelihood (ML) and Bayesian Inference (BI) phylogenetic trees based on the concatenated sequences of two mitochondrial genes (cytochrome oxidase c subunit 1 and 16S ribosomal RNA) and one nuclear gene (28S ribosomal RNA) fragments (1,586 bp) revealed a polyphyletic relationship in both genera compared to the outgroups of other genera from the tribe Indochinellini. Scabies songkramensis was clustered separately from the congeners, whereas R. humilis and R. pilata were grouped within the Scabies clade with high support (88% bootstrap support for ML and a Bayesian posterior probability of 1 for BI), and separated from other members of Radiatula from western Indochina (Myanmar and India). Based on these phylogenetic results, in combination with morphological and biogeographic data, these two Indochinese Radiatula species were transferred to Scabies, as S. humilis (Lea, 1856) comb. nov. and S. pilata (Lea, 1866) comb. nov. The genus Radiatula s.s. should be implied only to taxa endemic to the western Indochinese region, while the genus Scabies are distributed in the Chao Phraya and Mekong River basins and other rivers that drain into the Gulf of Thailand.
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Lydeard, C., Mulvey, M. and Davis, G.M. 1996. Molecular systematics and evolution of reproductive traits of North American freshwater unionacean mussels (Mollusca: Bivalvia) as inferred from 16S rRNA gene sequences. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 351: 1593-1603.
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Pfeiffer, J.M. and Graf, D.L. 2015. Evolution of bilaterally asymmetrical larvae in freshwater mussels (Bivalvia: Unionoida: Unionidae). Zoological Journal of the Linnean Society, 175(2): 307-318.
Pfeiffer, J.M., Graf, D.L., Cummings, K.S. and Page, L.M. 2018. Molecular phylogeny and taxonomic revision of two enigmatic freshwater mussel genera (Bivalvia: Unionidae incertae sedis: Harmandia and Unionetta) reveals a diverse clade of Southeast Asian Parreysiinae. Journal of Molluscan Studies, 84(4): 404-416.
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Silvestro, D. and Michalak, I. 2012. RaxmlGUI: A graphical front-end for RAxML. Organisms Diversity and Evolution, 12: 335-337.
Stamatakis, A. 2014. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30(9): 1312-1313.
Stecher, G., Kumar, S. and Tamura, K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution, 33(7): 1870-1874.
Strayer, D.l. 2008. Freshwater mussel ecology: A multifactor approach to distribution and abundance. Freshwater Ecology Series. University of California Press, California, 204 pp.
Tanabe, A.S. 2011. Kakusan4 and Aminosan: Two programs for comparing nonpartitioned, proportional and separate models for combined molecular phylogenetic analyses of multilocus sequence data. Molecular Ecology Resources, 11(5): 914-921.
Voris, H.K. 2000. Maps of Pleistocene sea levels in Southeast Asia: Shorelines, river systems and time durations. Journal of Biogeography, 27(5): 1153-1167.
Whelan, N.V., Geneva, A.J. and Graf, D.L. 2011. Molecular phylogenetic analysis of tropical freshwater mussels (Mollusca: Bivalvia: Unionoida) resolves the position of Coelatura and supports a monophyletic Unionidae. Molecular Phylogenetics and Evolution, 61(2): 504-514.
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AVMA 2013. AVMA guidelines for the euthanasia of animals. American Veterinary Medical Association.
Bogan, A. 2008. Global diversity of freshwater mussels (Mollusca, Bivalvia) in freshwater. Hydrobiologia, 595: 139-147.
Bolotov, I.N., Kondakov, A.V., Vikhrev, I.V., Aksenova, O.V., Bespalaya, Y.V., Gofarov, M.Y., Kolosova, Y.S., Konopleva, E.S., Spitsyn, V.M., Tanmuangpak, K. and Tumpeesuwan, S. 2017a. Ancient river inference explains exceptional oriental freshwater mussel radiations. Scientific Reports, 7(1): 2135.
Bolotov, I.N., Pfeiffer, J.M., Konopleva, E.S., Vikhrev, I.V., Kondakov, A.V., Aksenova, O.V., Gofarov, M.Y., Tumpeesuwan, S. and Win, T. 2018. A new genus and tribe of freshwater mussel (Unionidae) from Southeast Asia. Scientific Reports, 8(1): 10030.
Bolotov, I.N., Vikhrev, I.V., Kondakov, A.V., Konopleva, E.S., Gofarov, M.Y., Aksenova, O.V. and Tumpeesuwan, S. 2017b. New taxa of freshwater mussels (Unionidae) from a species-rich but overlooked evolutionary hotspot in Southeast Asia. Scientific Reports, 7(1): 11573.
Boyer, S.L., Howe, A.A., Juergens, N.W. and Hove, M.C. 2011. A DNA-barcoding approach to identifying juvenile freshwater mussels (Bivalvia:Unionidae) recovered from naturally infested fishes. Journal of the North American Benthological Society, 30(1): 182-194.
Brandt, R. 1974. The non-marine aquatic Mollusca of Thailand. Archiv fur Molluskenkunde, 105: 1-423.
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3(5): 294-299.
Graf, D.L. 2013. Patterns of freshwater bivalve global diversity and the state of phylogenetic studies on the Unionoida, Sphaeriidae, and Cyrenidae. American Malacological Bulletin, 31(1): 135-153.
Graf, D.L. and Cummings, K.S. 2007. Review of the systematics and global diversity of freshwater mussel species (Bivalvia: Unionoida). Journal of Molluscan Studies, 73(4): 291-314.
Graf, D.L. and Cummings, K.S. 2019. The Freshwater Mussels (Unionoida) of the World (and other less consequential bivalves). Retrieved from http:// mussel-project.uwsp.edu/ (accessed 13 March 2019).
Haag, W.R. and Williams, J.D. 2014. Biodiversity on the brink: An assessment of conservation strategies for North American freshwater mussels. Hydrobiologia, 735: 45-60.
Haas, F. 1969. Superfamilia Unionacea. Das Tierreich, 88: 1-663.
Hebert, P.D.N., Cywinska, A., Ball, S.L. and deWaard, J.R. 2003. Biological identifications through DNA barcodes. Proceedings of the Royal Society of London. Series B: Biological Sciences, 270(1512): 313-321.
Hutchison, C.S. 1989. Geological evolution of South-east Asia. Clarendon Press, Oxford.
Jeratthitikul, E., Phuangphong, S., Sutcharit, C., Prasankok, P., Kongim, B. and Panha, S. 2019. Integrative taxonomy reveals phenotypic plasticity in the freshwater mussel Contradens contradens (Bivalvia: Unionidae) in Thailand, with a description of a new species. Systematics and Biodiversity: 1-14.
Jovelin, R. and Justine, J.-L. 2001. Phylogenetic relationships within the polyopisthocotylean monogeneans (Platyhelminthes) inferred from partial 28S rDNA sequences. International Journal for Parasitology, 31(4): 393-401.
Köhler, F., Seddon, M., Bogan, A.E., Tu, D.V., Sri-Aroon, P. and Allen, D. 2012. The status and distribution of freshwater molluscs of the Indo-Burma region. In: D. Allen, K. Smith and W. Darwall (Editors), The Status and Distribution of Freshwater Biodiversity in Indo-Burma. IUCN, Cambridge, pp. 66-88.
Kongim, B., Sutcharit, C. and Panha, S. 2015. Cytotaxonomy of unionid freshwater mussels (Unionoida, Unionidae) from northeastern Thailand with description of a new species. Zookeys, 514: 93-110.
Konopleva, E.S., Bolotov, I.N., Vikhrev, I.V., Gofarov, M.Y. and Kondakov, A.V. 2017. An integrative approach underscores the taxonomic status of Lamellidens exolescens, a freshwater mussel from the Oriental tropics (Bivalvia: Unionidae). Systematics and Biodiversity, 15(3): 204-217.
Konopleva, E.S., Pfeiffer, J.M., Vikhrev, I.V., Kondakov, A.V., Gofarov, M.Y., Aksenova, O.V., Lunn, Z., Chan, N. and Bolotov, I.N. 2019. A new genus and two new species of freshwater mussels (Unionidae) from western Indochina. Scientific Reports, 9(1): 4106.
Lea, I. 1856. Description of twenty-five new species of exotic uniones. Proceedings of the Academy of Natural Sciences of Philadelphia, 8: 92-95.
Lea, I. 1857. Descriptions of exotic genera and species of the family Unionidæ [New fresh water and land shells]. Journal of the Academy of Natural Sciences, 3 [O. 6]: 289-321, pls. 21-33 (Obs. 6, part 1: 9-41).
Lea, I. 1866. Description of five new species of the genus Unio. Proceedings of the Academy of Natural Sciences of Philadelphia, 18: 133.
Lea, I. 1868. New Unionidæ, Melanidæ, etc., chiefly of the United States. Journal of the Academy of Natural Sciences, 6 [O. 12]: 249-302, pls. 29-45 (Obs. 12: 9-62).
Lydeard, C., Mulvey, M. and Davis, G.M. 1996. Molecular systematics and evolution of reproductive traits of North American freshwater unionacean mussels (Mollusca: Bivalvia) as inferred from 16S rRNA gene sequences. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 351: 1593-1603.
Miller, M., Pfeiffer, W. and Schwartz, T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees, Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, pp. 1-8.
Pfeiffer, J.M. and Graf, D.L. 2015. Evolution of bilaterally asymmetrical larvae in freshwater mussels (Bivalvia: Unionoida: Unionidae). Zoological Journal of the Linnean Society, 175(2): 307-318.
Pfeiffer, J.M., Graf, D.L., Cummings, K.S. and Page, L.M. 2018. Molecular phylogeny and taxonomic revision of two enigmatic freshwater mussel genera (Bivalvia: Unionidae incertae sedis: Harmandia and Unionetta) reveals a diverse clade of Southeast Asian Parreysiinae. Journal of Molluscan Studies, 84(4): 404-416.
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. and Huelsenbeck, J.P. 2012. MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space. Systematic Biology, 61(3): 539-542.
Silvestro, D. and Michalak, I. 2012. RaxmlGUI: A graphical front-end for RAxML. Organisms Diversity and Evolution, 12: 335-337.
Stamatakis, A. 2014. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30(9): 1312-1313.
Stecher, G., Kumar, S. and Tamura, K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution, 33(7): 1870-1874.
Strayer, D.l. 2008. Freshwater mussel ecology: A multifactor approach to distribution and abundance. Freshwater Ecology Series. University of California Press, California, 204 pp.
Tanabe, A.S. 2011. Kakusan4 and Aminosan: Two programs for comparing nonpartitioned, proportional and separate models for combined molecular phylogenetic analyses of multilocus sequence data. Molecular Ecology Resources, 11(5): 914-921.
Voris, H.K. 2000. Maps of Pleistocene sea levels in Southeast Asia: Shorelines, river systems and time durations. Journal of Biogeography, 27(5): 1153-1167.
Whelan, N.V., Geneva, A.J. and Graf, D.L. 2011. Molecular phylogenetic analysis of tropical freshwater mussels (Mollusca: Bivalvia: Unionoida) resolves the position of Coelatura and supports a monophyletic Unionidae. Molecular Phylogenetics and Evolution, 61(2): 504-514.
Woodward, F.R. 1969. The morphology of Ensidens ingallsianus (Lea, 1852) and Scabies crispata (Gould, 1843) (Bivalvia, Unionidae). Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening, 132: 49-62.
Zieritz, A., Lopes-Lima, M., Bogan, A.E., Sousa, R., Walton, S., Rahim, K.A.A., Wilson, J.-J., Ng, P.-Y., Froufe, E. and McGowan, S. 2016. Factors driving changes in freshwater mussel (Bivalvia, Unionida) diversity and distribution in Peninsular Malaysia. Science of The Total Environment, 571(Supplement C): 1069-1078.
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2019-03-31
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JERATTHITIKUL, E., SUCHARIT, C. and PRASANKOK, P. 2019. Molecular phylogeny of the Indochinese freshwater mussel genus Scabies Haas, 1911 (Bivalvia: Unionidae). Tropical Natural History. 19, 1 (Mar. 2019), 21–36.
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