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The species flocks of lacustrine gastropods: Tylomelania on Sulawesi as models in speciation and adaptive radiation

  • SPECIATION IN ANCIENT LAKES
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Abstract

Endemic radiations provide splendid opportunities for studies in evolutionary biology. Species flocks in ancient lakes, such as in Tanganyika, Malawi or Baikal, have featured prominently in evolutionary biology, viewing these “evolutionary theatres” as hotspots of diversification. However, following a century of neglect, the endemic evolution of limnic cerithioidean gastropods in the two central lake systems on the Indonesian island of Sulawesi (i.e. Lake Poso and the lakes of the Malili system, e.g. Danau Matano, Mahalona and Towuti) also provide instructive model cases for the study of speciation mechanisms, adaptive radiation and annidation (i.e. niche exploitation). We here discuss the evolutionary and taxonomic implications of the lacustrine species flocks in Tylomelania from these lakes in Sulawesi as an exceptional endemic assemblage of morphologically distinct viviparous pachychilid gastropods. This first comprehensive compilation of data on both ancient lake systems, Poso and Malili, offers a new perspective on ecological differentiation in this radiation. Presented here within the framework of the theory of evolutionary ecology it provides a research program for acquiring a synthetical perspective that includes morphology, molecular genetics, ecology and biogeography. In this context, it will be possible to compare the species flocks of these truly “Darwinian snails” on Sulawesi with the long enigmatic, so-called thalassoid (i.e. marine-like) gastropod radiation in East African’s Lake Tanganyika.

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References

  • Albrecht, C., S. Trajanovski, K. Kuhn, B. Streit & T. Wilke, 2006. Rapid evolution of an ancient lake species flock: freshwater limpets (Gastropoda: Ancylidae) in the Balkan Lake Ohrid. Organisms, Diversity & Evolution 6: 294–307.

    Article  Google Scholar 

  • Boss, K. J., 1978. On the evolution of gastropods in ancient lakes. In Fretter, V. & J. F. Peake (eds), Systematics, Evolution and Ecology, Vol. 2A. Academic Press, London: 385–428.

    Google Scholar 

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

    Google Scholar 

  • Davis, G. M., 1979. The origin and evolution of the gastropod family Pomatiopsidae with emphasis on the Mekong River Triculinae. Monographs of the Academy of Natural Sciences of Philadelphia 20: 1–120.

    Google Scholar 

  • Davis, G. M., 1982. Historical and ecological factors in the evolution, adaptive radiation, and biogeography of freshwater mollusks. American Zoologist 22: 375–395.

    Google Scholar 

  • Funk, D. J. & K. E. Omland, 2003. Species-level paraphyly and polyphyly: frequency, causes, and consequences, with Insights from animal mitochondrial DNA. Annual Review of Ecology and Systematics 34: 397–423.

    Article  Google Scholar 

  • Giesen, W., 1994. Indonesia’s major freshwater lakes: a review of current knowledge, development processes and threats. Mitteilungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 24: 115–128.

    Google Scholar 

  • Giesen, W., M. Baltzer & R. Baruadi, 1991. Integrating Conservation with Land-use Development in Wetlands of South Sulawesi. Directorate General of Forest Protection and Nature Conservation, Bogor.

  • Glaubrecht, M., 1996. Evolutionsökologie und Systematik am Beispiel von Süß- und Brackwasserschnecken (Mollusca: Caenogastropoda: Cerithioidea): Ontogenese-Strategien, paläontologische Befunde und historische Zoogeographie. Backhuys, Leiden: 499 pp.

  • Glaubrecht, M., 1999. Systematics and the evolution of viviparity in tropical freshwater gastropods (Cerithioidea: Thiaridae sensu lato)—an overview. Courier Forschungs-Institut Senckenberg 203: 91–96.

    Google Scholar 

  • Glaubrecht, M., 2000. A look back in time—toward an historical biogeography as a synthesis of systematic and geologic patterns outlined with limnic gastropods. Zoology 102: 127–147.

    Google Scholar 

  • Glaubrecht, M., 2004. Leopold von Buch’s legacy: treating species as dynamic natural entities, or why geography matters. American Malacological Bulletin 19: 111–134.

    Google Scholar 

  • Glaubrecht, M., 2006. Independent evolution of reproductive modes in viviparous freshwater Cerithioidea (Gastropoda, Sorbeoconcha)—a brief review. Basteria 69 (Suppl. 3): 32–38.

    Google Scholar 

  • Glaubrecht, M., 2008. Adaptive radiation of thalassoid Cerithioidean gastropods in Lake Tanganyika, East Africa: morphology and systematization of a paludomid species flock in an ancient lake. Zoosystematics and Evolution 84: 69–120.

    Google Scholar 

  • Glaubrecht, M. & F. Köhler, 2004. Radiating in a river: systematics, molecular genetics and morphological differentiation of viviparous freshwater gastropods endemic to the Kaek River, central Thailand (Cerithioidea, Pachychilidae). Biological Journal of the Linnean Society 82: 275–311.

    Article  Google Scholar 

  • Glaubrecht, M. & E. E. Strong, 2007. Ancestry to an endemic radiation in Lake Tanganyika? Evolution of the viviparous gastropod Potadomoides Leloup, 1953 in the Congo River system (Cerithioidea, Paludomidae). Biological Journal of the Linnean Society 92: 367–401.

    Article  Google Scholar 

  • Glaubrecht, M. & T. von Rintelen, 2003. Systematics and zoogeography of the pachychilid gastropod Pseudopotamis Martens, 1894 (Mollusca: Gastropoda: Cerithioidea): a limnic relict on the Torres Strait Islands, Australia? Zoologica Scripta 32: 415–435.

    Article  Google Scholar 

  • Haffner, G. D., P. E. Hehanussa & D. Hartoto, 2001. The biology and physical processes of large lakes of Indonesia: Lakes Matano and Towuti. In Munawar, M. & R. E. Hecky (eds), The Great Lakes of the World (GLOW): Food-Web Health and Integrity. Backhuys Publishers, Leiden: 183–192.

    Google Scholar 

  • Hawkins, S. J., D. C. Watson, A. S. Hill, P. Harding, M. A. Kyriakides, S. Hutchinson & T. A. Norton, 1989. A comparison of feeding mechanisms in microphageous, herbivorous, intertidal prosobranchs in relation to resource partitioning. Journal of Molluscan Studies 55: 151–165.

    Article  Google Scholar 

  • Herder, F., A. W. Nolte, J. Pfänder, J. Schwarzer, R. K. Hadiaty & U. K. Schliewen, 2006. Adaptive radiation and hybridization in Wallace’s dreamponds: evidence from sailfin silversides in the Malili lakes of Sulawesi. Proceedings of the Royal Society London B 273: 2209–2217.

    Article  Google Scholar 

  • Hutchinson, G. E., 1957. A Treatise on Limnology. Wiley, New York.

    Google Scholar 

  • Johannesson, K., E. Rolan-Alvarez & A. Ekendahl, 1995. Incipient reproductive isolation between two sympatric morphs of the intertidal snail Littorina saxatilis. Evolution 49: 1180–1190.

    Article  Google Scholar 

  • Köhler, F. & M. Glaubrecht, 2007. Out of Asia and into India: on the molecular phylogeny and biogeography of the endemic freshwater pachychilid gastropod Paracrostoma Cossmann, 1900 (Caenogastropoda: Pachychilidae). Biological Journal of the Linnean Society 91: 627–651.

    Article  Google Scholar 

  • Köhler, F., T. von Rintelen, A. Meyer & M. Glaubrecht, 2004. Multiple origin of viviparity in Southeast Asian gastropods (Cerithioidea: Pachychilidae) and its evolutionary implications. Evolution 58: 2215–2226.

    PubMed  Google Scholar 

  • Kottelat, M., 1990. Sailfin silversides (Pisces: Telmatherinidae) of Lakes Towuti, Mahalona and Wawontoa (Sulawesi, Indonesia) with descriptions of two new genera and two new species. Ichthyological Exploration of Freshwaters 1: 227–246.

    Google Scholar 

  • Kottelat, M., 1991. Sailfin silversides (Pisces: Telmatherinidae) of Lake Matano, Sulawesi, Indonesia, with descriptions of six new species. Ichthyological Exploration of Freshwaters 1: 321–344.

    Google Scholar 

  • Kottelat, M., A. J. Whitten, S. N. Kartikasari & S. Wirjoatmodjo, 1993. Freshwater Fishes of Western Indonesia and Sulawesi. Periplus, Jakarta.

    Google Scholar 

  • Kruimel, J. H., 1913. Verzeichnis der von Herrn E. C. Abendanon in Celebes gesammelten Süsswasser-Mollusken. Bijdragen tot de Dierkunde 19: 217–235.

    Google Scholar 

  • Kyle, C. J. & E. G. Boulding, 1998. Molecular genetic evidence for parallel evolution in a marine gastropod, Littorina subrotundata. Proceedings of the Royal Society London B 265: 303–308.

    Article  CAS  Google Scholar 

  • Lydeard, C., W. E. Holznagel, M. Glaubrecht & W. F. Ponder, 2002. Molecular phylogeny of a circum-global, diverse gastropod superfamily (Cerithioidea: Mollusca: Caenogastropoda): pushing the deepest phylogenetic limits of mitochondrial LSU rDNA sequences. Molecular Phylogenetics and Evolution 22: 399–406.

    Article  PubMed  CAS  Google Scholar 

  • Mayr, E., 1997. This is Biology. Belknap Press, Cambridge, MA.

    Google Scholar 

  • Mayr, E., 2004. What makes Biology Unique? Considerations on the Autonomy of a Scientific Discipline. Cambridge University Press, Cambridge, UK.

    Google Scholar 

  • Padilla, D. K., 1998. Inducible phenotypic plasticity of the radula in Lacuna (Gastropoda: Littorinidae). Veliger 4: 201–204.

    Google Scholar 

  • Reid, D. G., 2000. The use of the radula in the taxonomy and phylogeny of gastropods: cautionary cases of convergence, intraspecific variation and plasticity. Phuket Marine Biological Center Special Publication 21: 329–345.

    Google Scholar 

  • Reid, D. G. & Y. M. Mak, 1999. Indirect evidence for ecophenotypic plasticity in radular dentition of Littoraria species (Gastropoda: Littorinidae). Journal of Molluscan Studies 65: 355–370.

    Article  Google Scholar 

  • Rossiter, A. & H. Kawanabe (eds), 2000. Ancient Lakes: Biodiversity, Ecology and Evolution. Academic Press, San Diego.

    Google Scholar 

  • Salzburger, W. & A. Meyer, 2004. The species flocks of East African cichlid fishes: recent advances in molecular phylogenetics and population genetics. Naturwissenschaften 91: 277–290.

    Article  PubMed  CAS  Google Scholar 

  • Sarasin, P. & F. Sarasin, 1897. Über die Molluskenfauna der großen Süßwasser-Seen von Central-Celebes. Zoologischer Anzeiger 539(540): 308–320.

    Google Scholar 

  • Sarasin, P. & F. Sarasin, 1898. Die Süßwassermollusken von Celebes. Kreidel, Wiesbaden.

    Google Scholar 

  • Sarasin, P. & F. Sarasin, 1905. Reisen in Celebes ausgeführt in den Jahren 1893–1896 und 1902–1903. Kreidel, Wiesbaden.

    Google Scholar 

  • Schluter, D., 2000. The Ecology of Adaptive Radiation. Oxford University Press, Oxford.

    Google Scholar 

  • Seehausen, O., 2004. Hybridization and adaptive radiation. Trends in Ecology and Evolution 19: 198–207.

    Article  PubMed  Google Scholar 

  • Sites, J. W. & J. C. Marshall, 2004. Operational criteria for delimiting species. Annual Review of Ecology and Systematics 35: 199–227.

    Article  Google Scholar 

  • Streelman, J. T. & P. D. Danley, 2003. The stages of vertebrate evolutionary radiation. Trends in Ecology and Evolution 18: 126–131.

    Article  Google Scholar 

  • Sudhaus, W., 2004. Radiation within the framework of evolutionary ecology. Organisms, Diversity & Evolution 4: 127–134.

    Article  Google Scholar 

  • van Oosterzee, P., 1997. Where Worlds Collide. The Wallace line. Cornell University Press, Ithaca.

    Google Scholar 

  • von Rintelen, T., P. Bouchet & M. Glaubrecht, 2007. Ancient lakes as hotspots of diversity: a morphological review of an endemic species flock of Tylomelania (Gastropoda: Cerithioidea: Pachychilidae) in the Malili lake system on Sulawesi, Indonesia. Hydrobiologia 592: 11–94.

    Article  Google Scholar 

  • von Rintelen, T. & M. Glaubrecht, 2003. New discoveries in old lakes: three new species of Tylomelania Sarasin & Sarasin, 1897 (Gastropoda: Cerithioidea: Pachychilidae) from the Malili lake system on Sulawesi, Indonesia. Journal of Molluscan Studies 69: 3–17.

    Article  Google Scholar 

  • von Rintelen, T. & M. Glaubrecht, 2005. Anatomy of an adaptive radiation: a unique reproductive strategy in the endemic freshwater gastropod Tylomelania (Cerithioidea: Pachychilidae) on Sulawesi, Indonesia, and its biogeographic implications. Biological Journal of the Linnean Society 85: 513–542.

    Article  Google Scholar 

  • von Rintelen, T., A. B. Wilson, A. Meyer & M. Glaubrecht, 2004. Escalation and trophic specialization drive adaptive radiation of viviparous freshwater gastropods in the ancient lakes on Sulawesi, Indonesia. Proceedings of the Royal Society London B 271: 2541–2549.

    Article  Google Scholar 

  • Vogler, A. P. & M. T. Monaghan, 2006. Recent advances in DNA taxonomy. Journal of Zoological Systematics and Evolutionary Research 45: 1–10.

    Article  Google Scholar 

  • Wesenberg-Lund, C., 1939. Biologie der Süsswassertiere. Wirbellose Tiere. Julius Springer, Wien.

    Google Scholar 

  • Wilding, C. S., R. K. Butlin & J. Grahame, 2001. Differential gene-exchange between morphs of Littorina saxatilis detected using AFLP markers. Journal of Evolutionary Biology 14: 611–619.

    Article  CAS  Google Scholar 

  • Will, K. W. & D. Rubinoff, 2004. Myth of the molecule: DNA barcodes for species cannot replace morphology for identification and classification. Cladistics 20: 47–55.

    Article  Google Scholar 

  • Wilson, A. B., M. Glaubrecht & A. Meyer, 2004. Ancient lakes as evolutionary reservoirs: evidence from the thalassoid gastropods of Lake Tanganyika. Proceedings of the Royal Society London B 271: 529–536.

    Article  Google Scholar 

  • Wilson, M. E. J. & S. J. Moss, 1999. Cenozoic palaeogeographic evolution of Sulawesi and Borneo. Palaeogeography, Palaeoclimatology, Palaeoecology 145: 303–337.

    Article  Google Scholar 

  • Woltereck, R., 1931. Beobachtungen und Versuche zum Fragenkomplex der Artbildung. I. Wie entsteht eine endemische Rasse oder Art? Biologisches Zentralblatt 51: 231–253.

    Google Scholar 

  • Woltereck, R., 1941. Die Seen und Inseln der “Wallacea”-Zwischenregion und ihre endemische Tierwelt. Erster Teil: Vorgeschichte und Aufgabe der Forschungsreise. Internationale Revue der gesamten Hydrobiologie und Hydrographie 41: 1–36.

    Article  Google Scholar 

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Acknowledgements

We thank the editors for inviting us to present our findings not only during the 2006 SIAL meeting held in Berlin, but also for contributing this review to the special issue. Christian Albrecht and George Davis as reviewers and Tom Wilke provided constructive comments helping to improve the manuscript. We are most grateful to Kristina von Rintelen (Berlin) for her immense help both during the recent field campaigns and in analyzing data. Ristiyanti Marwoto (Zoological Museum Bogor) was very helpful in the preparation of the fieldwork in Indonesia and A. Munandar provided assistance in the field. We thank LIPI for permits to conduct research in Indonesia. We are most indebted to INCO for its invaluable logistic support at the lakes during our many visits. This work was funded by research grants GL 297/1 and GL 297/7 awarded to M. G. from the Deutsche Forschungsgemeinschaft.

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Correspondence to Matthias Glaubrecht.

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Guest editors: T. Wilke, R. Väinölä & F. Riedel

Patterns and Processes of Speciation in Ancient Lakes: Proceedings of the Fourth Symposium on Speciation in Ancient Lakes, Berlin, Germany, September 4–8, 2006

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Glaubrecht, M., von Rintelen, T. The species flocks of lacustrine gastropods: Tylomelania on Sulawesi as models in speciation and adaptive radiation. Hydrobiologia 615, 181–199 (2008). https://doi.org/10.1007/s10750-008-9568-9

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