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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

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Evolution in Action

Abstract

The study of species flocks in island settings such as ancient lakes can contribute significantly to our understanding of fundamental evolutionary processes, such as speciation, radiation, adaptation, and coevolution. We here use endemic freshwater gastropods in ancient lakes on the Indonesian island of Sulawesi as models to gain insights into patterns and mechanisms of lacustrine diversification. In two central lake systems on the island, i.e., Lake Poso and the five connected Malili lakes, the pachychilid freshwater snail genus Tylomelania has radiated into a diverse endemic assemblage of c. 53 species of morphologically distinct viviparous gastropods. Molecular phylogenetic data revealed that independent and multiple colonizations of the two lake systems by fluviatile ancestors have led to four morphologically and ecologically diverse adaptive radiations, one in Lake Poso and three in the Malili system. The evolution of habitat preferences and trophic specialization most likely drive diversification in both systems, while geography, i.e., allopatric speciation, is a major factor in the spatially strongly structured Malili system. Highly characteristic lacustrine shell forms have evolved in all lakes through escalation, i.e., coevolution with molluscivorous crabs. The role of the conspicuous body coloration present mainly in Lake Poso species remains to be elucidated, specifically its potential role in diversification processes. Finally, the setting of the Sulawesi snail species flocks with two independent radiations under almost identical extrinsic conditions offers insights into parallel patterns of adaptive evolution. However, a major conservation effort will be required to preserve the lakes’ spectacular species for future research.

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References

  • Abendanon EC (1915) Midden-Celebes-Expeditie. Geologische en geographische doorkruisingen van Midden-Celebes (1909–1910), Atlas. E.J. Brill, Leiden

    Google Scholar 

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

    Article  Google Scholar 

  • Albrecht C, Wilke T (2008) Ancient Lake Ohrid: biodiversity and evolution. Hydrobiologia 615:13–140

    Google Scholar 

  • Barlow GW (2000) The cichlid fishes: nature’s grand experiment in evolution. Perseus, Cambridge, Mass

    Google Scholar 

  • Bouchet P, Guerra A, Rolán E, Rocha F (1995) A major new mollusc radiation discovered in the ancient lakes of Sulawesi. In: Abstracts of the 12th International Malacological Congress, Vigo 1995, Vigo, pp 14–15

    Google Scholar 

  • Brooks JL (1950) Speciation in ancient lakes. Q Rev Biol 25:131–176

    Article  PubMed  CAS  Google Scholar 

  • Darwin C (1859) The origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. Murray, London

    Google Scholar 

  • Davis GM (1982) Historical and ecological factors in the evolution, adaptive radiation, and biogeography of freshwater mollusks. Am Zool 22:375–395

    Google Scholar 

  • Funk DJ, Omland KE (2003) Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annu Rev Ecol Syst 34:397–423

    Article  Google Scholar 

  • Giesen W (1994) Indonesia's major freshwater lakes: a review of current knowledge, development processes and threats. Mitt Int Verein Theoret Angew Limnol 24:115–128

    Google Scholar 

  • Giesen W, Baltzer M, Baruadi R (1991) Integrating conservation with land-use development in wetlands of South Sulawesi. Directorate General of Forest Protection and Nature Conservation, Bogor

    Google Scholar 

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

    Google Scholar 

  • 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. Am Malacol Bull 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. Zoosyst Evol 84:69–120

    Google Scholar 

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

    Article  Google Scholar 

  • Glaubrecht M, Strong EE (2007) Ancestry to an endemic radiation in Lake Tanganyika? Evolution of the viviparous gastropod Potadomoides Leloup, 1953 in the Congo River system (Cerithioidea, Paludomidae). Biol J Linn Soc 92:367–401

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Glaubrecht M, Rintelen T von (2008) The species flocks of lacustrine gastropods: Tylomelania on Sulawesi as models in speciation and adaptive radiation. Hydrobiologia 615:181–199

    Article  Google Scholar 

  • Gorthner A, Martens K, Goddeeris B, Coulter G (1994) What is an ancient lake? In: Martens K, Goddeeris B, Coulter G (eds) Speciation in ancient lakes. Schweizerbart'sche, Stuttgart, pp 97–100

    Google Scholar 

  • Grant PR (1998) Evolution on islands. Oxford University Press, Oxford

    Google Scholar 

  • Gray SM, Dill LM, Tantu FY, Loew ER, Herder F, McKinnon JS (2008) Environment-contingent sexual selection in a colour polymorphic fish. Proc R Soc Lond B 275:1785–1791

    Article  Google Scholar 

  • Haffner GD, Hehanussa PE, Hartoto D (2001) The biology and physical processes of large lakes of Indonesia: Lakes Matano and Towuti. In: Munawar M, Heck RE (eds) The Great Lakes of the world (GLOW): Food-web, health and integrity. Backhuys, Leiden, pp 183–192

    Google Scholar 

  • Hauswald AK, Albrecht C, Wilke T (2008) Testing two contrasting evolutionary patterns in ancient lakes: species flock versus species scatter in valvatid gastropods of Lake Ohrid. Hydrobiologia 615:169–179

    Article  Google Scholar 

  • Hawkins SJ, Watson DC, Hill AS, Harding P, Kyriakides MA, Hutchinson S, Norton TA (1989) A comparison of feeding mechanisms in microphageous, herbivorous, intertidal prosobranchs in relation to resource partitioning. J Molluscan Stud 55:151–165

    Article  Google Scholar 

  • Herder F, Nolte AW, Pfänder J, Schwarzer J, Hadiaty RK, Schliewen UK (2006a) Adaptive radiation and hybridization in Wallace’s dreamponds: evidence from sailfin silversides in the Malili lakes of Sulawesi. Proc R Soc Lond B 273:2209–2217

    Article  Google Scholar 

  • Herder F, Schwarzer J, Pfänder J, Hadiaty RK, Schliewen UK (2006b) Preliminary checklist of sailfin silversides (Telostei: Telmatherinidae) in the Malili Lakes of Sulawesi (Indonesia), with a synopsis of systematics and threats. Verh Ges Ichthyol 5:139–163

    Google Scholar 

  • Herder F, Pfänder J, Schliewen UK (2008) Adaptive sympatric speciation of polychromatic “roundfin” sailfin silverside fish in Lake Matano (Sulawesi). Evolution 62:2178–2195

    Article  PubMed  Google Scholar 

  • Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267

    Article  PubMed  CAS  Google Scholar 

  • Hutchinson GE (1965) The ecological theater and the evolutionary play. Yale University Press, New Haven

    Google Scholar 

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

    Article  Google Scholar 

  • Kocher TD (2004) Adaptive evolution and explosive speciation: the cichlid fish model. Nature Rev Genet 5:288–298

    Article  PubMed  CAS  Google Scholar 

  • Köhler F, Glaubrecht M (2007) Out of Asia and into India: on the molecular phylogeny and biogeography of the endemic freshwater pachychilid gastropod Paracrostoma Cossmann, 1900 (Caenogastropoda: Pachychilidae). Biol J Linn Soc 91:627–651

    Article  Google Scholar 

  • Köhler F, Glaubrecht M (2010) Uncovering an overlooked radiation: morphological and mitochondrial DNA differentiation in endemic freshwater snails on Madagascar (Caenogastropoda: Pachychilidae) and their biogeography. Biol J Linn Soc 99:867–894

    Google Scholar 

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

    PubMed  Google Scholar 

  • Kornfield I, Smith PF (2000) African cichlid fishes: model systems for evolutionary biology. Annu Rev Ecol Syst 31:163–196

    Article  Google Scholar 

  • Kruimel JH (1913) Verzeichnis der von Herrn E.C.Abendanon in Celebes gesammelten Süsswasser-Mollusken. Bijdr Dierk 19:217–235

    Google Scholar 

  • Kyle CJ, Boulding EG (1998) Molecular genetic evidence for parallel evolution in a marine gastropod, Littorina subrotundata. Proc R Soc Lond B 265:303–308

    Article  CAS  Google Scholar 

  • Marijnissen SAE, Michel E, Daniels SR, Erpenbeck D, Menken SBJ, Schram FR (2006) Molecular evidence for recent divergence of Lake Tanganyika endemic crabs (Decapoda: Platythelphusidae). Mol Phylogenet Evol 40:628–634

    Article  PubMed  CAS  Google Scholar 

  • Martens K (1997) Speciation in ancient lakes. Trends Ecol Evol 12:177–182

    Article  PubMed  CAS  Google Scholar 

  • Marwoto R (1997) A preliminary study of the biodiversity of the freshwater snail family Thiaridae from Indonesia (Mollusca: Prosobranchia). In: Ulrich H (ed) Tropical biodiversity and systematics. Zoologisches Forschungsinstitut und Museum Alexander Koenig, Bonn, pp 109–112

    Google Scholar 

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

    Google Scholar 

  • Reid DG (2000) The use of the radula in the taxonomy and phylogeny of gastropods: cautionary cases of convergence, intraspecific variation and plasticity. Phuket Mar Biol Center Spec Publ 21:329–345

    Google Scholar 

  • Reid DG, Mak YM (1999) Indirect evidence for ecophenotypic plasticity in radular dentition of Littoraria species (Gastropoda: Littorinidae). J Molluscan Stud 65:355–370

    Article  Google Scholar 

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

    Google Scholar 

  • Rintelen T von, Glaubrecht M (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. Biol J Linn Soc 85:513–542

    Google Scholar 

  • Rintelen T von, Glaubrecht M (2008) Three new species of the freshwater snail genus Tylomelania (Caenogastropoda: Pachychilidae) from the Malili lake system, Sulawesi, Indonesia. Zootaxa 1852:37–49

    Google Scholar 

  • Rintelen T von, Wilson AB, Meyer A, Glaubrecht M (2004) Escalation and trophic specialization drive adaptive radiation of viviparous freshwater gastropods in the ancient lakes on Sulawesi, Indonesia. Proc R Soc Lond B 271:2541–2549

    Google Scholar 

  • Rintelen T von, Bouchet P, Glaubrecht M (2007a) 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 592:1–94

    Google Scholar 

  • Rintelen K von, Rintelen T von, Glaubrecht M (2007b) Molecular phylogeny and diversification of freshwater shrimps (Decapoda, Atyidae, Caridina) from ancient Lake Poso (Sulawesi, Indonesia) – The importance of being colourful. Mol Phylogenet Evol 45:1033–1041

    Google Scholar 

  • Rintelen, K von, Glaubrecht M, Schubart CD, Wessel A, Rintelen T von (in press) Adaptive radiation and ecological diversification of Sulawesi’s ancient lake shrimps. Evolution

    Google Scholar 

  • Rossiter A, Kawanabe H (eds) (2000) Ancient lakes: biodiversity, ecology and evolution. Academic, San Diego

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Sarasin P, Sarasin F (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 

  • Schubart CD, Ng PKL (2008) A new molluscivore crab from Lake Poso confirms multiple colonisation of ancient lakes in Sulawesi by freshwater crabs (Decapoda: Brachyura). Zool J Linn Soc 154:211–221

    Article  Google Scholar 

  • Schubart CD, Santl T, Koller P (2008) Mitochondrial patterns of intra- and interspecific differentiation among endemic freshwater crabs of ancient lakes in Sulawesi. Contr Zool 77:83–90

    Google Scholar 

  • Schultheiß R, Albrecht C, Bößneck U, Wilke T (2008) The neglected side of speciation in ancient lakes: phylogeography of an inconspicuous mollusc taxon in lakes Ohrid and Prespa. Hydrobiologia 615:141–156

    Article  Google Scholar 

  • Schwarzer J, Herder F, Misof B, Hadiaty RK, Schliewen UK (2008) Gene flow at the margin of Lake Matano’s adaptive sailfin silverside radiation: Telmatherinidae of River Petea in Sulawesi. Hydrobiologia 615:201–213

    Article  CAS  Google Scholar 

  • Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecol Evol 19:198–207

    Article  PubMed  Google Scholar 

  • Seehausen O, Terai Y, Magalhaes IS, Carleton KL, Mrosso HDJ, Miyagi R, van der Sluijs I, Schneider MV, Maan ME, Tachida H, Imai H, Okada N (2008) Speciation through sensory drive in cichlid fish. Nature 455:620–626

    Article  PubMed  CAS  Google Scholar 

  • Sites JW, Marshall JC (2004) Operational criteria for delimiting species. Annu Rev Ecol Syst 35:199–227

    Article  Google Scholar 

  • Streelman JT, Danley PD (2003) The stages of vertebrate evolutionary radiation. Trends Ecol Evol 18:126–131

    Article  Google Scholar 

  • van Oosterzee P (1997) Where worlds collide. The Wallace line. Cornell University Press, Ithaca

    Google Scholar 

  • Vogler AP, Monaghan MT (2006) Recent advances in DNA taxonomy. J Zool Syst Evol Res 45:1–10

    Article  Google Scholar 

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

    Book  Google Scholar 

  • Whittaker RJ, Fernández-Palacios JM (2007) Island biogeography. Ecology, evolution, and conservation. Oxford University Press, Oxford

    Google Scholar 

  • Wilding CS, Butlin RK, Grahame J (2001) Differential gene-exchange between morphs of Littorina saxatilis detected using AFLP markers. J Evol Biol 14:611–619

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Wilson MEJ, Moss SJ (1999) Cenozoic palaeogeographic evolution of Sulawesi and Borneo. Palaeogeogr Palaeoclimatol 145:303–337

    Article  Google Scholar 

  • Wilson AB, Glaubrecht M, Meyer A (2004) Ancient lakes as evolutionary reservoirs: evidence from the thalassoid gastropods of Lake Tanganyika. Proc R Soc Lond B 271:529–536

    Article  Google Scholar 

  • Woltereck R (1931) Beobachtungen und Versuche zum Fragenkomplex der Artbildung. I. Wie entsteht eine endemische Rasse oder Art? Biol Zentralbl 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. Int Rev Ges Hydrobiol Hydrogr 41:1–36

    Article  Google Scholar 

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Acknowledgments

We thank Ristiyanti Marwoto (Zoological Museum Bogor) who was very helpful in the preparation of the fieldwork in Indonesia and A. Munandar who 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. Claudia Dames, Betina Gregor, Tanja Miethe, Jutta Simonis (Museum für Naturkunde Berlin), Janice Jang (Massachusetts Institute of Technology) and Daniela Franz (Technische Universität Dresden) were of great help in collecting genetic and morphological data from both ancient lake systems. 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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Appendix 1.

Appendix 1.

Species of Tylomelania described from the ancient lakes of Sulawesi and species diversity estimates for the lakes and the entire island (based on Rintelen and Glaubrecht 2003; Rintelen and Glaubrecht 2008; Rintelen et al. 2007a; unpublished data)

Region/Taxon (*=not endemic)

No. of species

Sulawesi

N = 44 + c. 32 undescribed

Malili lake system

n = 28

Lake Matano

n = 7 (6 endemic)

T. gemmifera Sarasin and Sarasin 1897

 

T. matannensis Rintelen et al. 2007a

 

T. molesta Sarasin and Sarasin 1897

 

*T. palicolarum Sarasin and Sarasin 1897

 

T. patriarchalis Sarasin and Sarasin 1897

 

T. turriformis Rintelen et al. 2007a

 

T. zeamais Sarasin and Sarasin 1897

 

Lake Mahalona

n = 9 (4 endemic)

T. confusa Rintelen et al. 2007a

 

T. hannelorae Rintelen and Glaubrecht 2008

 

T. inconspicua Rintelen et al. 2007a

 

*T. insulaesacrae Sarasin and Sarasin 1897

 

T. kruimeli Rintelen and Glaubrecht 2003

 

*T. mahalonensis Kruimel 1913

 

*T. marwotoae Rintelen et al. 2007a

 

*T. palicolarum Sarasin and Sarasin 1897

 

*T. wolterecki Rintelen et al. 2007a

 

Tominanga river

n = 4 (1 endemic)

*T. tominangensis Kruimel 1913

 

*T. mahalonensis Kruimel 1913

 

*T. towutica Kruimel 1913

 

T. wesseli Rintelen et al. 2007a

 

Lake Towuti

n = 10 (6 endemic)

T. amphiderita Rintelen et al. 2007a

 

T. bakara Rintelen and Glaubrecht 2003

 

*T. insulaesacrae Sarasin and Sarasin 1897

 

T. kristinae Rintelen et al. 2007a

 

T. lalemae Kruimel 1913

 

*T. marwotoae Rintelen et al. 2007a

 

T. sarasinorum Kruimel 1913

 

T. towutensis Sarasin and Sarasin 1897

 

*T. towutica Kruimel 1913

 

*T. wolterecki Rintelen et al. 2007a

 

Lake Lontoa

n = 2 (1 endemic)

T. abendanoni Kruimel 1913

 

*T. tominangensis Kruimel 1913

 

Lake Masapi

n = 1 (endemic)

T. masapensis Kruimel 1913

 

Larona River

n = 2 (endemic)

T. baskasti Rintelen and Glaubrecht 2008

 

T. sinabartfeldi Rintelen and Glaubrecht 2008

 

Lake Poso

n = 7 + c. 18 undescribed

Lake Poso

n = 4 + c. 10 undescribed

T. carbo Sarasin and Sarasin 1897

 

T. centaurus Sarasin and Sarasin 1898

 

T. kuli Sarasin and Sarasin 1898

 

T. toradjarum Sarasin and Sarasin 1897

 

Poso River

n = 3 + c. 8 undescribed

T. connectens Sarasin and Sarasin 1898

 

T. neritiformis Sarasin and Sarasin 1897

 

T. porcellanica Sarasin and Sarasin 1897

 

Rivers

n = 9 + c. 14 undescribed

div. Tylomelania species (not listed here in detail)

 

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von Rintelen, T., von Rintelen, K., Glaubrecht, M. (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. (eds) Evolution in Action. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-12425-9_23

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