, Volume 615, Issue 1, pp 181–199 | Cite as

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

  • Matthias Glaubrecht
  • Thomas von Rintelen


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.


Freshwater gastropods Speciation Adaptive radiation Molecular phylogeny Evolutionary ecology 



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.


  1. 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.CrossRefGoogle Scholar
  2. 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
  3. Brooks, J. L., 1950. Speciation in ancient lakes. Quarterly Review of Biology 25: 30–60, 131–176.Google Scholar
  4. 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
  5. 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
  6. 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.CrossRefGoogle Scholar
  7. 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
  8. 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.Google Scholar
  9. 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.Google Scholar
  10. 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
  11. 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
  12. 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
  13. 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
  14. 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
  15. 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.CrossRefGoogle Scholar
  16. 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.CrossRefGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. 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
  19. 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.CrossRefGoogle Scholar
  20. 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.CrossRefGoogle Scholar
  21. Hutchinson, G. E., 1957. A Treatise on Limnology. Wiley, New York.Google Scholar
  22. 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.CrossRefGoogle Scholar
  23. 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.CrossRefGoogle Scholar
  24. 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.PubMedGoogle Scholar
  25. 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
  26. 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
  27. Kottelat, M., A. J. Whitten, S. N. Kartikasari & S. Wirjoatmodjo, 1993. Freshwater Fishes of Western Indonesia and Sulawesi. Periplus, Jakarta.Google Scholar
  28. 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
  29. 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.CrossRefGoogle Scholar
  30. 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.PubMedCrossRefGoogle Scholar
  31. Mayr, E., 1997. This is Biology. Belknap Press, Cambridge, MA.Google Scholar
  32. Mayr, E., 2004. What makes Biology Unique? Considerations on the Autonomy of a Scientific Discipline. Cambridge University Press, Cambridge, UK.Google Scholar
  33. Padilla, D. K., 1998. Inducible phenotypic plasticity of the radula in Lacuna (Gastropoda: Littorinidae). Veliger 4: 201–204.Google Scholar
  34. 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
  35. 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.CrossRefGoogle Scholar
  36. Rossiter, A. & H. Kawanabe (eds), 2000. Ancient Lakes: Biodiversity, Ecology and Evolution. Academic Press, San Diego.Google Scholar
  37. 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.PubMedCrossRefGoogle Scholar
  38. Sarasin, P. & F. Sarasin, 1897. Über die Molluskenfauna der großen Süßwasser-Seen von Central-Celebes. Zoologischer Anzeiger 539(540): 308–320.Google Scholar
  39. Sarasin, P. & F. Sarasin, 1898. Die Süßwassermollusken von Celebes. Kreidel, Wiesbaden.Google Scholar
  40. Sarasin, P. & F. Sarasin, 1905. Reisen in Celebes ausgeführt in den Jahren 1893–1896 und 1902–1903. Kreidel, Wiesbaden.Google Scholar
  41. Schluter, D., 2000. The Ecology of Adaptive Radiation. Oxford University Press, Oxford.Google Scholar
  42. Seehausen, O., 2004. Hybridization and adaptive radiation. Trends in Ecology and Evolution 19: 198–207.PubMedCrossRefGoogle Scholar
  43. Sites, J. W. & J. C. Marshall, 2004. Operational criteria for delimiting species. Annual Review of Ecology and Systematics 35: 199–227.CrossRefGoogle Scholar
  44. Streelman, J. T. & P. D. Danley, 2003. The stages of vertebrate evolutionary radiation. Trends in Ecology and Evolution 18: 126–131.CrossRefGoogle Scholar
  45. Sudhaus, W., 2004. Radiation within the framework of evolutionary ecology. Organisms, Diversity & Evolution 4: 127–134.CrossRefGoogle Scholar
  46. van Oosterzee, P., 1997. Where Worlds Collide. The Wallace line. Cornell University Press, Ithaca.Google Scholar
  47. 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.CrossRefGoogle Scholar
  48. 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.CrossRefGoogle Scholar
  49. 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.CrossRefGoogle Scholar
  50. 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.CrossRefGoogle Scholar
  51. Vogler, A. P. & M. T. Monaghan, 2006. Recent advances in DNA taxonomy. Journal of Zoological Systematics and Evolutionary Research 45: 1–10.CrossRefGoogle Scholar
  52. Wesenberg-Lund, C., 1939. Biologie der Süsswassertiere. Wirbellose Tiere. Julius Springer, Wien.Google Scholar
  53. 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.CrossRefGoogle Scholar
  54. 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.CrossRefGoogle Scholar
  55. 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.CrossRefGoogle Scholar
  56. Wilson, M. E. J. & S. J. Moss, 1999. Cenozoic palaeogeographic evolution of Sulawesi and Borneo. Palaeogeography, Palaeoclimatology, Palaeoecology 145: 303–337.CrossRefGoogle Scholar
  57. 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
  58. 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.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  1. 1.Museum für NaturkundeHumboldt University BerlinBerlinGermany

Personalised recommendations