Molecular phylogeny reveals a new genus of freshwater mussels from the Mekong River Basin (Bivalvia: Unionidae)

  • Ekgachai Jeratthitikul Animal Systematics and Molecular Ecology Laboratory, Department of Biology, Faculty of Science, Mahidol University, Bangkok 10400, Thailand https://orcid.org/0000-0002-3477-9548
  • Chirasak Sutcharit Animal Systematics Research Unit, Department of Biology, Faculty of Science, Chulalongkorn University, Bangkok 10330, Thailand https://orcid.org/0000-0001-7670-9540
  • Peng Bun Ngor Faculty of Fisheries, Royal University of Agriculture, Khan Dongkor, P.O. Box 2696, Phnom Penh, 12401, Cambodia and Wonders of the Mekong Project, c/o Inland Fisheries Research and Development Institute (IFReDI), no. 86, Norodom Boulevard., PO Box 582, Phnom Penh, Cambodia. https://orcid.org/0000-0002-3659-6577
  • Pongpun Prasankok School of Biology, Institute of Science, Suranaree University of Technology, Nakhon Ratchasima 30000, Thailand https://orcid.org/0000-0001-5967-223X
Keywords: Indochina, freshwater mussels, multi-locus phylogeny, new taxa, time-calibrated phylogeny

Abstract

A new genus of freshwater mussels (Bivalvia: Unionidae) is described from the Mekong River Basin as Namkongnaia gen. nov. The validity of the new genus is supported by its unique conchological characteristics, namely the lack of hinge dentition and elongated shells, together with its evolutionary distinctiveness as estimated by multi-locus phylogenetic analyses (mitochondrial COI and 16S, and nuclear 28S genes). The new genus includes two lineages with deep divergence, shown by 5.10% uncorrected COI p-distance. One lineage is a type species described herein as Namkongnaia inkhavilayi gen. et sp. nov. The other is a recognized species under the name ‘Pilsbryoconcha lemeslei (Morelet, 1875)’. Molecular phylogenetic analysis further shows that the new genus belongs to the tribe Pseudodontini, and evolutionarily is closely related to the genus Monodontina Conrad, 1853. However, its conchology is similar to the genus Pilsbryoconcha Simpson, 1900. Time-calibrated phylogeny suggests that the main radiation events of the tribe Pseudodontini occurred during the Late Cretaceous to the Eocene, with the divergence between the new genus and Monodontina placed in the Miocene. The discovery of new freshwater mussel taxa in this study highlights the importance of the Mekong River Basin as one of the world’s biodiversity hotspots for freshwater fauna.

References

Abell R., Thieme M.L., Revenga C., Bryer M., Kottelat M., Bogutskaya N., Coad B., Mandrak N., Balderas S.C., Bussing W., Stiassny M.L.J., Skelton P., Allen G.R., Unmack P., Naseka A., Ng R., Sindorf N., Robertson J., Armijo E., Higgins J.V., Heibel T.J., Wikramanayake E., Olson D., López H.L., Reis R.E., Lundberg J.G., Sabaj Pérez M.H. & Petry P. 2008. Freshwater ecoregions of the World: A new map of biogeographic units for freshwater biodiversity conservation. BioScience 58 (5): 403–414. https://doi.org/10.1641/B580507

AVMA 2020. AVMA guidelines for the euthanasia of animals. American Veterinary Medical Association. Available from https://www.avma.org/sites/default/files/2020-01/2020-Euthanasia-Final-1-17-20.pdf [accessed 12 May 2021].

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. & Tumpeesuwan S. 2017a. Ancient river inference explains exceptional oriental freshwater mussel radiations. Scientific Reports 7: 2135. https://doi.org/10.1038/s41598-017-02312-z

Bolotov I.N., Vikhrev I.V., Kondakov A.V., Konopleva E.S., Gofarov M.Y., Aksenova O.V. & 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. https://doi.org/10.1038/s41598-017-11957-9

Bolotov I.N., Pfeiffer J.M., Konopleva E.S., Vikhrev I.V., Kondakov A.V., Aksenova O.V., Gofarov M.Y., Tumpeesuwan S. & Win T. 2018. A new genus and tribe of freshwater mussel (Unionidae) from Southeast Asia. Scientific Reports 8 (1): 10030. https://doi.org/10.1038/s41598-018-28385-y

Bolotov I.N., Konopleva E.S., Vikhrev I.V., Gofarov M.Y., Lopes-Lima M., Bogan A.E., Lunn Z., Chan N., Win T., Aksenova O.V., Tomilova A.A., Tanmuangpak K., Tumpeesuwan S. & Kondakov A.V. 2020. New freshwater mussel taxa discoveries clarify biogeographic division of Southeast Asia. Scientific Reports 10 (1): 6616. https://doi.org/10.1038/s41598-020-63612-5

Bouckaert R., Vaughan T.G., Barido-Sottani J., Duchêne S., Fourment M., Gavryushkina A., Heled J., Jones G., Kühnert D., De Maio N., Matschiner M., Mendes F.K., Müller N.F., Ogilvie H.A., du Plessis L., Popinga A., Rambaut A., Rasmussen D., Siveroni I., Suchard M.A., Wu C.H., Xie D., Zhang C., Stadler T. & Drummond A.J. 2019. BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Computational Biology 15 (4): e1006650. https://doi.org/10.1371/journal.pcbi.1006650

Brandt R.A.M. 1974. The non-marine aquatic Mollusca of Thailand. Archiv für Molluskenkunde 105: 1–423.

Buerki S., Forest F., Stadler T. & Alvarez N. 2013. The abrupt climate change at the Eocene-Oligocene boundary and the emergence of South-East Asia triggered the spread of sapindaceous lineages. Annals of Botany 112 (1): 151–160. https://doi.org/10.1093/aob/mct106

Carmichael M.J., Inglis G.N., Badger M.P.S., Naafs B.D.A., Behrooz L., Remmelzwaal S., Monteiro F.M., Rohrssen M., Farnsworth A., Buss H.L., Dickson A.J., Valdes P.J., Lunt D.J. & Pancost R.D. 2017. Hydrological and associated biogeochemical consequences of rapid global warming during the Paleocene-Eocene Thermal Maximum. Global and Planetary Change 157: 114–138. https://doi.org/https://doi.org/10.1016/j.gloplacha.2017.07.014

Coates D., Poeu O., Suntornratana U., Tung N.T. & Viravong S. 2003. Biodiversity and Fisheries in the Lower Mekong Basin. Mekong Development Series no. 2. Mekong River Commission, Phnom Penh. Available from https://www.mrcmekong.org/assets/Publications/report-management-develop/Mek-Dev-No2-Mek-River-Biodiversityfiisheries-in.pdf [accessed 12 May 2021].

Conrad T.A. 1853. A synopsis of the family of Naïades of North America, with notes, and a table of some of the genera and sub-genera of the family, according to their geographical distribution, and descriptions of genera and sub-genera. Proceedings of the Academy of Natural Sciences of Philadelphia 6: 243–269. Available from https://www.biodiversitylibrary.org/page/1779779 [accessed 12 May 2021].

Crosse H. & Fischer P. 1876. Mollusques fluviatiles, recueillis au Cambodge, par la mission scientifique francaise de 1873. Journal de Conchyliologie 24: 313–342. Available from https://www.biodiversitylibrary.org/page/16071628 [accessed 12 May 2021].

Darriba D., Taboada G.L., Doallo R. & Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9 (8): 772. https://doi.org/10.1038/nmeth.2109

Do V.T., Tuan L.Q. & Bogan A.E. 2018. Freswater mussels (Bivalvia: Unionida) of Vietnam: diversity, distribution, and cobservation status. Freshwater Mollusk Biology and Conservation 21: 1–18. https://doi.org/10.31931/fmbc.v21i1.2018.1-18

Drummond A.J., Ho S.Y.W., Phillips M.J. & Rambaut A. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biology 4 (5): e88. https://doi.org/10.1371/journal.pbio.0040088

Folmer O., Black M., Hoeh W., Lutz R. & 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.

Fonseca M.M., Lopes-Lima M., Eackles M.S., King T.L. & Froufe E. 2016. The female and male mitochondrial genomes of Unio delphinus and the phylogeny of freshwater mussels (Bivalvia: Unionida). Mitochondrial DNA Part B 1 (1): 954–957. https://doi.org/10.1080/23802359.2016.1241677

Frierson L. 1927. A Classified and Annotated Check List of the North American Naiades. Baylor University Press, Waco, Texas.

Froufe E., Bolotov I.N., Aldridge D.C., Bogan A.E., Breton S., Gan H.M., Kovitvadhi U., Kovitvadhi S., Riccardi N., Secci-Petretto G., Sousa R., Teixeira A., Varandas S., Zanatta D., Zieritz A., Fonseca M.M. & Lopes-Lima M. 2020. Mesozoic mitogenome rearrangements and freshwater mussel (Bivalvia: Unionoidea) macroevolution. Heredity 124 (1): 182–196. https://doi.org/10.1038/s41437-019-0242-y

Graf D.L. & 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. https://doi.org/10.1093/mollus/eym029

Graf D.L. & Cummings K.S. 2021a. A ‘big data’ approach to global freshwater mussel diversity (Bivalvia: Unionoida), with an updated checklist of genera and species. Journal of Molluscan Studies 87 (1). https://doi.org/10.1093/mollus/eyaa034

Graf D.L. & Cummings K.S. 2021b. The freshwater mussels (Unionoida) of the World (and other less consequential bivalves). Available from http://mussel-project.uwsp.edu/index.html [accessed 12 May 2021].

Haas F. 1920. Die Unioniden. In: Küster H.C. (ed.) Systematisches Conchylien-Cabinet von Martini und Chemnitz 9 (pt. 2, h. 52): 289–304. Available from https://www.biodiversitylibrary.org/page/34419468 [accessed 12 May 2021].

Haas F. 1969a. Superfamilia Unionacea. In: Martens R. & Hennig W. (eds) Das Tierreich, Lieferung 88. Walter de Gruyter, Berlin.

Haas F. 1969b. Superfamily Unionacea Fleming, 1828. In: Moore R.C. (ed.) Treatise on Invertebrate Paleontology: N411–N470. Geological Society of America and the University of Kansas, Lawrence, Kansas.

Huang X.C., Su J.H., Ouyang J.X., Ouyang S., Zhou C.H. & Wu X.P. 2019. Towards a global phylogeny of freshwater mussels (Bivalvia: Unionida): Species delimitation of Chinese taxa, mitochondrial phylogenomics, and diversification patterns. Molecular Phylogenetics and Evolution 130: 45–59. https://doi.org/https://doi.org/10.1016/j.ympev.2018.09.019

Huelsenbeck J.P. & Hillis D.M. 1993. Success of phylogenetic methods in the four-taxon case. Systematic Biology 42 (3): 247–264. https://doi.org/10.1146/annurev.ecolsys.28.1.437

Jeratthitikul E., Phuangphong S., Sutcharit C., Prasankok P., Kongim B. & Panha S. 2019a. 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 17 (2): 134–147. https://doi.org/10.1080/14772000.2018.1554607

Jeratthitikul E., Sucharit C. & Prasankok P. 2019b. Molecular phylogeny of the Indochinese freshwater mussel genus Scabies Haas, 1911 (Bivalvia: Unionidae). Tropical Natural History 19: 21–36. Available from https://li01.tci-thaijo.org/index.php/tnh/article/view/181195 [accessed 12 May 2021].

Jovelin R. & 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. https://doi.org/10.1016/S0020-7519(01)00114-X

Kang B. & Huang X. 2021. Mekong fishes: Biogeography, migration, resources, threats, and conservation. Reviews in Fisheries Science & Aquaculture: 1–38. https://doi.org/10.1080/23308249.2021.1906843

Köhler F., Seddon M., Bogan A.E., Do V.T., Sri-Aroon P. & Allen D. 2012. The status and distribution of freshwater molluscs of the Indo-Burma region. In: Allen D.J., Smith K.G. & Darwall W.R.T. (eds) The Status and Distribution of Freshwater Biodiversity in Indo-Burma: 66-88. IUCN, Cambridge.

Kongim B., Sutcharit C. & Panha S. 2015. Cytotaxonomy of unionid freshwater mussels (Unionoida, Unionidae) from northeastern Thailand with description of a new species. ZooKeys 514: 93–110. https://doi.org/10.3897/zookeys.514.8977

Konopleva E.S., Bolotov I.N., Spitsyn V.M., Kondakov A.V., Gofarov M.Y. & Vikhrev I.V. 2019. A new Contradens from Laos (Bivalvia: Unionidae: Contradentini). Ecologica Montenegrina 24: 25–31.

https://doi.org/10.37828/em.2019.24.5

Konopleva E.S., Bolotov I.N., Pfeiffer J.M., Vikhrev I.V., Kondakov A.V., Gofarov M.Y., Tomilova A.A., Tanmuangpak K. & Tumpeesuwan S. 2021. New freshwater mussels from two Southeast Asian genera Bineurus and Thaiconcha (Pseudodontini, Gonideinae, Unionidae). Scientific Reports 11: 8244. https://doi.org/10.1038/s41598-021-87633-w

Kumar S., Stecher G. & Tamura K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33 (7): 1870–1874. https://doi.org/10.1093/molbev/msw054

Lanfear R., Frandsen P.B., Wright A.M., Senfeld T. & Calcott B. 2016. PartitionFinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34 (3): 772–773. https://doi.org/10.1093/molbev/msw260

Larget B. & Simon D.L. 1999. Markov Chasin Monte Carlo Algorithms for the Bayesian analysis of phylogenetic trees. Molecular Biology and Evolution 16 (6): 750–759. https://doi.org/10.1093/oxfordjournals.molbev.a026160

Lopes-Lima M., Froufe E., Do V.T., Ghamizi M., Mock K.E., Kebapçı Ü., Klishko O., Kovitvadhi S., Kovitvadhi U., Paulo O.S., Pfeiffer J.M., Raley M., Riccardi N., Şereflişan H., Sousa R., Teixeira A., Varandas S., Wu X., Zanatta D.T., Zieritz A. & Bogan A.E. 2017. Phylogeny of the most species-rich freshwater bivalve family (Bivalvia: Unionida: Unionidae): Defining modern subfamilies and tribes. Molecular Phylogenetics and Evolution 106: 174–191. https://doi.org/10.1016/j.ympev.2016.08.021

Lopes-Lima M., Burlakova L.E., Karatayev A.Y., Mehler K., Seddon M. & Sousa R. 2018. Conservation of freshwater bivalves at the global scale: diversity, threats and research needs. Hydrobiologia 810 (1): 1–14. https://doi.org/10.1007/s10750-017-3486-7

Lydeard C., Mulvey M. & 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 (1347): 1593–1603. https://doi.org/10.1098/rstb.1996.0143

Miller M.A., Pfeiffer W. & Schwartz T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees, 2010. Gateway Computing Environments Workshop (GCE): 1–8. https://doi.org/10.1109/GCE.2010.5676129

Modell H. 1942. Das natürliche System der Najaden. Archiv für Molluskenkunde 74: 161–191. Available https://www.zobodat.at/pdf/Archiv-fuer-Molluskenkunde_174_0161-0191.pdf [accessed 12 May 2021].

Morelet A. 1875. Séries conchyliologiques: Comprenant l’énumération de Mollusques terrestres et fluviatiles recueillis pendant le cours de différents voyages ainsi que la description de plusieurs espèces nouvelles 4. Klincksieck, Paris. Available from https://www.biodiversitylibrary.org/page/11913380 [accessed 12 May 2021].

Morlet L. 1889. Catalogue des coquilles recueillies, par M. Pavie, dans le Cambodge et le Royaume de Siam, et description d'espèces nouvelles. Journal de Conchyliologie 37 (2): 121–199. Available from https://www.biodiversitylibrary.org/page/16015483 [accessed 12 May 2021].

Muanta S., Jeratthitikul E., Panha S. & Prasankok P. 2019. Phylogeography of the freshwater bivalve genus Ensidens (Unionidae) in Thailand. Journal of Molluscan Studies 85 (2): 224–231. https://doi.org/10.1093/mollus/eyz013

Ng T.H., Jeratthitikul E., Sutcharit C., Chhuoy S., Pin K., Pholyotha A., Siriwut W., Srisonchai R., Hogan Z.S. & Ngor P.B. 2020. Annotated checklist of freshwater molluscs from the largest freshwater lake in Southeast Asia. ZooKeys 958: 107–141. https://doi.org/10.3897/zookeys.958.53865

Ngor P.B., Sor R., Prak L.H., So N., Hogan Z.S. & Lek S. 2018. Mollusc fisheries and length-weight relationship in Tonle Sap flood pulse system, Cambodia. Annales de Limnologie-International Journal of Limnology 54: 34–10. https://doi.org/10.1051/limn/2018026

Pfeiffer J.M. & 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. https://doi.org/10.1111/zoj.12282

Pfeiffer J.M., Graf D.L., Cummings K.S. & 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. https://doi.org/10.1093/mollus/eyy028

Pfeiffer J.M., Breinholt J.W. & Page L.M. 2019. Unioverse: A phylogenomic resource for reconstructing the evolution of freshwater mussels (Bivalvia, Unionoida). Molecular Phylogenetics and Evolution 137: 114–126. https://doi.org/10.1016/j.ympev.2019.02.016

Pfeiffer J.M., Graf D.L., Cummings K.S. & Page L.M. 2021. Taxonomic revision of a radiation of Southeast Asian freshwater mussels (Unionidae: Gonideinae: Contradentini+Rectidentini). Invertebrate Systematics 35 (4): 394–470. https://doi.org/10.1071/IS20044

Rambaut A., Drummond A.J., Xie D., Baele G. & Suchard M.A. 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67 (5): 901–904. https://doi.org/10.1093/sysbio/syy032

Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., Höhna S., Larget B., Liu L., Suchard M.A. & 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. https://doi.org/10.1093/sysbio/sys029

Simpson C.T. 1914. A Descriptive Catalogue of the Naiades, or Pearly fresh-water mussels. Parts I–III. Bryant Walker, Detroit, Michigan. Available from https://www.biodiversitylibrary.org/page/11344898 [accessed 12 May 2021].

Stamatakis A. 2014. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30 (9): 1312–1313. https://doi.org/10.1093/bioinformatics/btu033

Subba Rao N.V. 1989. Handbook,Freshwater Molluscs of India. Zoological Survey of India, Calcutta, India. Available from http://faunaofindia.nic.in/PDFVolumes/hpg/030/index.pdf [accessed 12 May 2021].

Thach N.N. 2007. Recently Collected Shells of Vietnam. L’Informatore Piceno and N.N.T, Ancona, Italy.

Wang Y., Zheng J., Zhang W., Li S., Liu X., Yang X. & Liu Y. 2012. Cenozoic uplift of the Tibetan Plateau: Evidence from the tectonic–sedimentary evolution of the western Qaidam Basin. Geoscience Frontiers 3 (2): 175–187. https://doi.org/10.1016/j.gsf.2011.11.005

Whelan N.V., Geneva A.J. & 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. https://doi.org/10.1016/j.ympev.2011.07.016

Zhang P., Najman Y., Mei L., Millar I., Sobel E.R., Carter A., Barfod D., Dhuime B., Garzanti E., Govin G., Vezzoli G. & Hu X. 2019. Palaeodrainage evolution of the large rivers of East Asia, and Himalayan-Tibet tectonics. Earth-Science Reviews 192: 601–630. https://doi.org/10.1016/j.earscirev.2019.02.003

Zieritz A., Bogan A.E., Froufe E., Klishko O., Kondo T., Kovitvadhi U., Kovitvadhi S., Lee J.H., Lopes-Lima M., Pfeiffer J.M., Sousa R., Van Do T., Vikhrev I. & Zanatta D.T. 2018. Diversity, biogeography and conservation of freshwater mussels (Bivalvia: Unionida) in East and Southeast Asia. Hydrobiologia 810 (1): 29–44. https://doi.org/10.1007/s10750-017-3104-8

Zieritz A., Froufe E., Bolotov I.N., Gonçalves D.V., Aldridge D.C., Bogan A.E., Gan H.M., Gomes-Dos-Santos A., Sousa R., Teixeira A., Varandas S., Zanatta D. & Lopes-Lima M. 2020. Mitogenomic phylogeny and fossil-calibrated mutation rates for all F- and M-type mtDNA genes of the largest freshwater mussel family, the Unionidae (Bivalvia). Zoological Journal of the Linnean Society: zlaa153. https://doi.org/10.1093/zoolinnean/zlaa153

Published
2021-10-22
How to Cite
Jeratthitikul, E., Sutcharit, C. ., Ngor, P. B., & Prasankok, P. (2021). Molecular phylogeny reveals a new genus of freshwater mussels from the Mekong River Basin (Bivalvia: Unionidae). European Journal of Taxonomy, 775(1), 119-142. https://doi.org/10.5852/ejt.2021.775.1553
Section
Research article