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Forgotten for decades: Lake Lanao and the genetic assessment of its mollusc diversity

  • SPECIATION IN ANCIENT LAKES 7
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Abstract

Lake Lanao on Mindanao island is the largest freshwater lake in the Philippines and may represent one of the few ancient lakes in Southeast Asia. This lake’s fauna is best known for its endemic cyprinid fishes that have been nearly driven to extinction through various anthropogenic actions. In contrast, only little is known about Lake Lanao’s invertebrate fauna and its placement within related Southeast Asian taxa. We here focus on the diversity in freshwater molluscs, particularly the morphologically diverse viviparid gastropods, and provide first genetic insights into this group in order to test whether the morphological variability observed is also reflected by corresponding genetic variation. Mitochondrial sequence data indicate that these viviparids form a monophyletic group comprising morphologically distinct and partly genetically different (morpho)species. Both the high diversity found in cyprinid fishes and viviparid gastropods together with the geological and tectonic evolution of Mindanao suggest that Lake Lanao may have originated more than 100,000 years ago and is thus indeed an ancient lake. However, its fauna is under continuous threat not least from the introduction of non-native species, and the development and implementation of sustainable conservation strategies is direly needed.

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References

  • Adam, B., 2010. L’Anodonte chinoise Sinanodonta woodiana (Lea, 1834) (Mollusca, Bivalvia, Unionidae): une espèce introduite qui colonise le bassin Rhône-Méditerranée. MalaCo 6: 278–287.

    Google Scholar 

  • Albrecht, C., O. Kroll, E. Moreno Terrazas & T. Wilke, 2009. Invasion of ancient Lake Titicaca by the globally invasive Physa acuta (Gastropoda: Pulmonata: Hygrophila). Biological Invasions 11: 1821–1826.

    Google Scholar 

  • Albrecht, C., K. Föller, C. Clewing, T. Hauffe & T. Wilke, 2014. Invaders versus endemics: alien gastropod species in ancient Lake Ohrid. Hydrobiologia 739: 163–174.

    Google Scholar 

  • Bartsch, P., 1907. The Philippine pond snails of the genus Vivipara. Proceedings of the United States National Museum 32: 135–150.

    Google Scholar 

  • Bartsch, P., 1909. Notes on the Philippine pond snails of the genus Vivipara, with descriptions of new species. Proceedings of the United States National Museum 37: 365–367.

    Google Scholar 

  • Bolotov, I. N., Y. V. Bespalaya, M. Y. Gofarov, A. V. Kondakov, E. S. Konopleva & I. V. Vikhrev, 2016. Spreading of the Chinese pond mussel, Sinanodonta woodiana, across Wallacea: one or more lineages invade tropical islands and Europe. Biochemical Systematics and Ecology 67: 58–64.

    CAS  Google Scholar 

  • Brooks, J. L., 1950. Speciation in ancient lakes. Quarterly Review of Biology 25(30–60): 131–176.

    CAS  PubMed  Google Scholar 

  • Burch, J. B., 1984. Freshwater snails of the Philippines. Walkerana 2: 81–112.

    Google Scholar 

  • Clement, M., D. Posada & K. A. Crandall, 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1659.

    CAS  PubMed  Google Scholar 

  • Cohen, A. S., 2012. Scientific drilling and biological evolution in ancient lakes: lessons learned and recommendations for the future. Hydrobiologia 682: 3–25.

    CAS  Google Scholar 

  • Cristescu, M. E., S. J. Adamowicz, J. J. Vaillant & G. D. Haffner, 2010. Ancient lakes revisited: from the ecology to the genetics of speciation. Molecular Ecology 19: 4837–4851.

    PubMed  Google Scholar 

  • Du, L., J. Yang, T. Rintelen, X. Chen & D. Aldridge, 2013. Molecular phylogenetic evidence that the Chinese viviparid genus Margarya (Gastropoda: Viviparidae) is polyphyletic. Chinese Science Bulletin 58: 2154–2162.

    CAS  Google Scholar 

  • Folmer, O., M. Black, W. Hoeh, R. Lutz & R. Vrijenhoek, 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.

    CAS  PubMed  Google Scholar 

  • Frey, D. G., 1969. A limnological reconnaissance of Lake Lanao. Verhandlungen des Internationalen Verein Limnologie 17: 1090–1102.

    Google Scholar 

  • Genner, M. J., E. Michel, D. Erpenbeck, N. de Voogd, F. Witte & J. P. Pointier, 2004. Camouflaged invasion of Lake Malawi by an Oriental gastropod. Molecular Ecology 13: 2135–2141.

    CAS  PubMed  Google Scholar 

  • Glaubrecht, M., N. Brinkmann & J. Pöppe, 2009. Diversity and disparity “down under”: systematics, biogeography and reproductive modes of the “marsupial” freshwater Thiaridae (Caenogastropoda, Cerithioidea) in Australia. Zoosystematics and Evolution 85: 199–275.

    Google Scholar 

  • Gorthner, A., 1994. What is an ancient lake? In Martens, K., G. Coulter & B. Goddeeris (eds), Speciation in Ancient Lakes. E.Schweizerbart’sche Verlagsbuchhandlung, Stuttgart: 97–100.

    Google Scholar 

  • Greenwood, P. H., 1984. What is a species flock? In Echelle, A. A. & I. Kornfield (eds), Evolution of Fish Species Flocks. University of Maine Press, Orono: 13–19.

    Google Scholar 

  • Haas, F., 1939. Malacological notes. Zoological Series of Field Museum of Natural History 24: 93–103.

    Google Scholar 

  • Hall, R., 1996. Reconstructing Cenozoic SE Asia. In Hall, R. & D. J. Blundell (eds), Geological Society, London, Special Publications. Geological Society, London: 153–184.

    Google Scholar 

  • Herre, A. W. C. T., 1924. Distribution of the true fresh-water fishes in the Philippines. I. The Philippine Cyprinidae. Philippine Journal of Science 24: 249–307.

    Google Scholar 

  • Herre, A. W. C. T., 1926. Two new fishes from Lake Lanao. Philippine Journal of Science 29: 499–503.

    Google Scholar 

  • Herre, A. W. C. T., 1932. Five new Philippine fishes. Copeia 1932: 139–142.

    Google Scholar 

  • Ismail, G. B., D. B. Sampson & D. L. G. Noakes, 2014. The status of Lake Lanao endemic cyprinids (Puntius species) and their conservation. Environmental Biology of Fishes 97: 425–434.

    Google Scholar 

  • Köhler, F., M. Seddon, A. E. Bogan, V. T. Do, P. Sri-Aroon & D. Allen, 2012. The status and distribution of freshwater molluscs of the Indo-Burma region. In Allen, D. J., K. G. Smith & W. R. T. Darwall (eds), The Status and Distribution of Freshwater Biodiversity in Indo-Burma. IUCN, Cambridge: 67–89.

    Google Scholar 

  • Kroll, O., R. Hershler, C. Albrecht, E. M. Terrazas, R. Apaza, C. Fuentealba, C. Wolff & T. Wilke, 2012. The endemic gastropod fauna of Lake Titicaca: correlation between molecular evolution and hydrographic history. Ecology and Evolution 2: 1517–1530.

    PubMed  PubMed Central  Google Scholar 

  • Kumar, S., G. Stecher & K. Tamura, 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33: 1870–1874.

    CAS  PubMed  Google Scholar 

  • Lee, T., S. Siripattrawan, F. Ituarte & D. O. Foighil, 2003. Invasion of the clonal clams: Corbicula lineages in the New World. American Malacological Bulletin 20: 113–122.

    Google Scholar 

  • Martens, K., 1997. Speciation in ancient lakes. Trends in Ecology & Evolution 12: 177–182.

    CAS  Google Scholar 

  • Messager, M. L., B. Lehner, G. Grill, I. Nedeva & O. Schmitt, 2016. Estimating the volume and age of water stored in global lakes using a geo-statistical approach. Nature Communications 7: 13603.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Michel, E., 1994. Why Snails Radiate: A Review of Gastropod Evolution in Long-Lived Lakes, Both Recent and Fossil Speciation in Ancient Lakes. E. Schweitzerbart’sche Verlagsbuchhandlung, Stuttgart: 284–317.

    Google Scholar 

  • Myers, G. S., 1960. The endemic fish fauna of Lake Lanao, and the evolution of higher taxonomic categories. Evolution 14: 323–333.

    Google Scholar 

  • Palumbi, S. R., D. M. Hillis, C. Moritz & B. K. Mable, 1996. Nucleic Acids II: The Polymerase Chain Reaction. Molecular Systematics. Sinauer, Sunderland: 205–247.

    Google Scholar 

  • PHIVOLCS, 2015. Distribution of Active Faults and Trenches in the Philippines. Department of Science and Technology (DOST), Philippine Institute of Volcanology and Seismology (PHIVOLCS), Quezon.

    Google Scholar 

  • Pigneur, L.-M., J. Marescaux, K. Roland, E. Etoundi, J.-P. Descy & K. Van Doninck, 2011. Phylogeny and androgenesis in the invasive Corbicula clams (Bivalvia, Corbiculidae) in Western Europe. BMC Evolutionary Biology 11: 147.

    PubMed  PubMed Central  Google Scholar 

  • Pubellier, M., R. Quebral, C. Rangin, B. Deffontaines, C. Muller, J. Butterlin & J. Manzano, 1991. The Mindanao Collision Zone: a soft collision event within a continuous Neogene strike-slip setting. Journal of Southeast Asian Earth Sciences 6: 239–248.

    Google Scholar 

  • QGIS Development Team, 2017. QGIS Geographic Information System. Open Source Geospatial Foundation Project. https://www.qgis.org/en/site.

  • Rosagaron, R. R., 2001. Lake Lanao: its past and present status. In Santiago, C. B., M. L. Cuvin-Aralar & Z. U. Basiao (eds), Conservation and Ecological Management of Philippine Lakes in Relation to Fisheries and Aquaculture. SEAFDEC, Bangkok: 29–39.

    Google Scholar 

  • Rossiter, A. & H. Kawanabe, 2000. Ancient Lakes: Biodiversity, Ecology and Evolution. Advances in Ecological Research. Academic Press, San Diego.

    Google Scholar 

  • Salzburger, W., B. Van Bocxlaer & A. S. Cohen, 2014. Ecology and evolution of the African Great Lakes and their faunas. Annual Review of Ecology, Evolution and Systematics 45: 519–545.

    Google Scholar 

  • Santos-Borja, A. C., 1994. The control of saltwater intrusion into Laguna de Bay: socioeconomic and ecological significance. Lake and Reservoir Management 10: 213–219.

    Google Scholar 

  • Schön, I. & K. Martens, 2004. Adaptive, pre-adaptive and non-adaptive components of radiations in ancient lakes: a review. Organisms Diversity and Evolution 4: 137–156.

    Google Scholar 

  • Schön, I., C. Poux, E. Verheyen & K. Martens, 2014. High cryptic diversity and persistent lineage segregation in endemic Romecytheridea (Crustacea, Ostracoda) from the ancient Lake Tanganyika (East Africa). Hydrobiologia 739: 119–131.

    Google Scholar 

  • Schultheiß, R., T. Wilke, A. Jørgensen & C. Albrecht, 2011. The birth of an endemic species flock: demographic history of the Bellamya group (Gastropoda, Viviparidae) in Lake Malawi. Biological Journal of the Linnean Society 102: 130–143.

    Google Scholar 

  • Seehausen, O., 2006. African cichlid fish: a model system in adaptive radiation research. Proceedings of the Royal Society of London B 273: 1987–1998.

    Google Scholar 

  • Sherbakov, D. Y., 1999. Molecular phylogenetic studies on the origin of biodiversity in Lake Baikal. Trends in Ecology & Evolution 14: 92–95.

    Google Scholar 

  • Shu, F., F. Köhler, C. Fu & H. Wang, 2013. A new species of Gyraulus (Gastropoda: Planorbidae) from ancient Lake Lugu, Yunnan-Guizhou Plateau, Southwest China. Molluscan Research 33: 34–39.

    Google Scholar 

  • Stelbrink, B., A. A. Shirokaya, K. Föller, T. Wilke & C. Albrecht, 2016. Origin and diversification of Lake Ohrid’s endemic acroloxid limpets: the role of geography and ecology. BMC Evolutionary Biology 16: 273.

    PubMed  PubMed Central  Google Scholar 

  • Strong, E., O. Gargominy, W. Ponder & P. Bouchet, 2008. Global diversity of gastropods (Gastropoda; Mollusca) in freshwater. Hydrobiologia 595: 149–166.

    Google Scholar 

  • Vaillant, J. J., G. D. Haffner & M. E. Cristecu, 2011. The ancient lakes of Indonesia: towards integrated research on speciation. Integrative and Comparative Biology 51: 634–643.

    PubMed  Google Scholar 

  • Vermeij, G. J. & A. P. Covich, 1978. Coevolution of freshwater gastropods and their predators. American Naturalist 112: 833–843.

    Google Scholar 

  • von Rintelen, T., K. von Rintelen & M. Glaubrecht, 2010. The species flocks of the viviparous freshwater gastropod Tylomelania (Mollusca: Cerithioidea: Pachychilidae) in the ancient lakes of Sulawesi, Indonesia: the role of geography, trophic morphology and color as driving forces in adaptive radiation. In Glaubrecht, M. (ed.), Evolution in Action. Springer, Berlin: 485–512.

    Google Scholar 

  • von Rintelen, T., K. von Rintelen, M. Glaubrecht, C. D. Schubart & F. Herder, 2012. Aquatic biodiversity hotspots in Wallacea: the species flocks in the ancient lakes of Sulawesi, Indonesia. In Gower, D. J., K. G. Johnson, J. E. Richardson, B. R. Rosen, L. Rüber & S. T. Williams (eds), Biotic evolution and environmental change in Southeast Asia. Cambridge University Press, Cambridge: 290–315.

    Google Scholar 

  • Wagner, B. & T. Wilke, 2011. Evolutionary and geological history of the Balkan lakes Ohrid and Prespa. Biogeosciences 8: 995–998.

    Google Scholar 

  • West, K. & A. S. Cohen, 1996. Shell microstructure of gastropods from Lake Tanganyika, Africa: adaptation, convergent evolution, and escalation. Evolution 50: 672–681.

    PubMed  Google Scholar 

  • Winnepenninckx, B., T. Backeljau & R. De Wachter, 1993. Extraction of high molecular weight DNA from molluscs. Trends in Genetics 9: 407.

    CAS  PubMed  Google Scholar 

  • Woltereck, R., 1941. Die Seen und Inseln der “Wallacea”-Zwischenregion und ihre endemische Tierwelt. Zweiter Teil: Inseln und Seen der Philippinen. Internationale Revue der Hydrobiologie 41: 37–176.

    Google Scholar 

  • Yumul, G. P., C. B. Dimalanta, V. B. Maglambayarw & E. J. Marquez, 2008. Tectonic setting of a composite terrane: a review of the Philippine island arc system. Geosciences Journal 12: 7–17.

    CAS  Google Scholar 

  • Zhang, Z., S. Schwartz, L. Wagner & W. Miller, 2000. A greedy algorithm for aligning DNA sequences. Journal of Computational Biology 7: 203–214.

    CAS  PubMed  Google Scholar 

  • Zhang, L.-J., S.-C. Chen, L.-T. Yang, L. Jin & F. Köhler, 2015. Systematic revision of the freshwater snail Margarya Nevill, 1877 (Mollusca: Viviparidae) endemic to the ancient lakes of Yunnan, China, with description of new taxa. Zoological Journal of the Linnean Society 174: 760–800.

    Google Scholar 

  • Zielske, S., M. Glaubrecht & M. Haase, 2011. Origin and radiation of rissooidean gastropods (Caenogastropoda) in ancient lakes of Sulawesi. Zoologica Scripta 40: 221–237.

    Google Scholar 

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

    Google Scholar 

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Acknowledgements

We particularly thank H.O. Faisal, A.B. Magarang, A.E. Mangondaya and L.G. Serad (SALLAM, Inc.), H.W. Macaayong, H.R.M. Naga and M.-S. Naga (Mindanao State University, Marawi City, Philippines), S.R.K. Adiong and B.A. Mamainte Jr. (Al Khalifa Foundation, Inc.) and P.M. Papandayan (Environment & Natural Resources Office, Province of Lanao des Sur) for their hospitality and logistic support at Lake Lanao. Moreover, we are grateful to M. Santos (National Museum of the Philippines, Manila, Philippines), who helped handling the loan of the material. We thank A.E. Bogan (North Carolina Museum of Natural Sciences, Raleigh, USA) and M. Lopes-Lima (University of Porto, Porto, Portugal) for the identification of the juvenile specimens of Sinanodonta woodiana. We further thank E. Strong (National Museum of Natural History, Smithsonian Institution, Washington, USA) for providing additional information on Paul Bartsch’s material and high-quality scans of his published plates. We also thank the editor and two anonymous reviewers for the positive feedback and constructive comments. This work was supported by the German Research Foundation (Deutsche Forschungsgemeinschaft, DFG) Grants STE 2460/1-1 and STE 2460/2-1 to B. Stelbrink.

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  1. Department of Animal Ecology and Systematics, Justus Liebig University Giessen, Heinrich-Buff-Ring 26-32 (IFZ), 35392, Giessen, Germany

    Björn Stelbrink, Christian Albrecht & Catharina Clewing

  2. Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, Invalidenstr. 43, 10115, Berlin, Germany

    Thomas von Rintelen

  3. Environment & Natural Resources Office, Province of Lanao des Sur, Buadi Sacayo, 9700, Marawi, Philippines

    Pipälawan O. Naga

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  1. Björn Stelbrink
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Correspondence to Björn Stelbrink.

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Stelbrink, B., von Rintelen, T., Albrecht, C. et al. Forgotten for decades: Lake Lanao and the genetic assessment of its mollusc diversity. Hydrobiologia 843, 31–49 (2019). https://doi.org/10.1007/s10750-018-3666-0

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