Adaptive sympatric speciation of polychromatic "roundfin" sailfin silverside fish in Lake Matano (Sulawesi)

Evolution

Volumn 62, Issue 9, 2008, Pages 2178-2195

  Herder, Fabian ^a,b   Pfaender, Jobst ^a   Schliewen, Ulrich K ^b  

^a ZOOLOGISCHES FORSCHUNGSMUSEUM ALEXANDER KOENIG   (Germany)

^b ZOOLOGISCHE STAATSSAMMLUNG MÜNCHEN   (Germany)

Author keywords

Adaptive radiation; Amplified fragment length polymorphism (AFLP); Malili Lakes; Natural selection; Sexual selection; Telmatherina sp. (Telmatherinidae)

Indexed keywords

ADAPTIVE RADIATION; ASSORTATIVE MATING; BODY SHAPE; COLOR MORPH; DIVERGENCE; EVOLUTIONARY BIOLOGY; GENE FLOW; LAKE ECOSYSTEM; MORPHOTYPE; REPRODUCTIVE ISOLATION; SEXUAL SELECTION; SPECIATION (BIOLOGY); SYMPATRY; TELEOST;

ADAPTATION; ANIMAL; ARTICLE; ECOSYSTEM; FEMALE; FISH; GENETIC SELECTION; GENETICS; HISTOLOGY; INDONESIA; MALE; PHENOTYPE; PIGMENTATION; POPULATION DYNAMICS; SEXUAL BEHAVIOR; SPECIES DIFFERENTIATION;

ADAPTATION, BIOLOGICAL; ANIMALS; ECOSYSTEM; FEMALE; FISHES; GENETIC SPECIATION; INDONESIA; MALE; PHENOTYPE; PIGMENTATION; POPULATION DYNAMICS; SELECTION (GENETICS); SEXUAL BEHAVIOR, ANIMAL;

ASIA; EURASIA; INDONESIA; LAKE MATANO; MALILI LAKES; SOUTH SULAWESI; SOUTHEAST ASIA;

ARGENTINA ELONGATA; TELMATHERINA; TELMATHERINIDAE;

EID: 51249113037     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2008.00447.x     Document Type: Article

References (85)

1. Angers, B., P. Magnan, M. Plante, and L. Bernatchez. 1999. Canonical correspondence analysis for estimating spatial and environmental effects on microsatellite gene diversity in brook charr (Salvelinus fontinalis). Mol. Ecol. 8 : 1043 1053.
2. Arnold, M. L. 1997. Natural hybridisation and evolution. Oxford Univ. Press, New York.
3. ST tell us? Trends. Ecol. Evol. 20 : 435 440.
4. Beaumont, M. A., and D. J. Balding. 2004. Identifying adaptive genetic divergence among populations from genome scans. Mol. Ecol. 13 : 969 980.
5. Beaumont, M., and R. A. Nichols. 1996. Evaluating loci for use in the genetic analysis of population structure. Proc. R. Soc. Lond. B 263 : 1619 1626.
6. Berlocher, S. H., and J. L. Feder. 2002. Sympatric speciation in phytophagous insects: moving beyond controversy? Annu. Rev. Entomol. 47 : 773 815.
7. Bonin, A., P. Taberlet, C. Miaud, and F. Pompanon. 2006. Explorative genome scan to detect candidate loci for adaptation along a gradient of altitude in the common frog (Rana temporaria). Mol. Biol. Evol. 24 : 773 783.
8. Bush, G. L. 1994. Sympatric speciation in animals: new wine in old bottles. Trends Ecol. Evol. 9 : 285 288.
9. Campbell, D., and L. Bernatchez. 2004. Generic scan using AFLP markers as a means to assess the role of directional selection in the divergence of sympatric whitefish ecotypes. Mol. Biol. Evol. 21 : 945 956.
10. Campbell, D., P. Duchesne, and L. Bernatchez. 2003. AFLP utility for population assignment studies: analytical investigation and comparison with microsatellites. Mol. Ecol. 12 : 1979 1991.
11. Chunco, A. J., J. S. McKinnon, and M. R. Servedio. 2007. Microhabitat variation and sexual selection can maintain male color polymorphisms. Evolution Online Early 23-Aug-2007. doi :.
12. Coyne, J. A. 2007. Sympatric speciation. Curr. Biol. 17 : R787 R788.
13. Coyne, J. A., and H. A. Orr. 2004. Speciation. Sinauer Associates, Sunderland, MA.
14. Crowe, S. A., A. H. O'Neill, S. Katsev, P. Hehanussa, G. D. Haffner, B. Sundby, A. Mucci, and D. Fowle. 2008. The biogeochemistry of tropical lakes: a case study from Lake Matano, Indonesia. Limnol. Oceanogr. 53 : 319 331.
15. Danley, P. D., and T. Kocher. 2001. Speciation in rapidly diverging systems: lessons from Lake Malawi. Mol. Ecol. 10 : 1075 1086.
16. Dieckmann, U., and M. Doebeli. 1999. On the origin of species by sympatric speciation. Nature 400 : 354 357.
17. Doebeli, M., and U. Dieckmann. 2000. Evolutionary branching and sympatric speciation caused by different types of ecological interactions. Am. Nat. 156 : S77 S101.
18. Doebeli, M., and U. Dieckmann. 2003. Speciation along environmental gradients. Nature 421 : 259 264.
19. Duchesne, P., and L. Bernatchez. 2002. AFLPOP: a computer program for simulated and real population allocation, based on AFLP data. Mol. Ecol. Notes 2 : 380 383.
20. Emelianov, I., F. E. Marec, and J. Mallet. 2004. Genomic evidence for divergence with gene flow in host races of the larch budmoth. Proc. R. Soc. Lond. B 271 : 97 105.
21. Excoffier, L., P. Smouse, and J. Quattro. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131 : 479 491.
22. Excoffier, L., G. Laval, and S. Schneider. 2005. Arlequin ver. 3.0: an integrated software package for population genetic data analysis. Evol. Bioinform. Online 1 : 47 50.
23. Feder, J. L. 1998. The Apple Maggot Fly, Rhagoletis pomonella: flies in the face of conventional wisdom about speciation? In : D. J. Howard, and S. H. Berlocher, eds. Species and speciation. Univ. Press, New York and Oxford.
24. Feder, J. L., X. Xie, J. Rull, S. Velez, A. Forbes, B. Leung, H. Dambroski, K. E. Filchak, and M. Aluja. 2005. Mayr, Dobzhanski, and Bush and the complexities of sympatric speciation in Rhagoletis. Proc. Natl. Acad. Sci. USA 102 : 6573 6580.
25. Friesen, V. L., A. L. Smith, E. Gómez-Diaz, M. Bolton, R. W. Furness, J. González-Solis, and L. R. Monteiro. 2007. Sympatric speciation by allochrony in a seabird. Proc. Natl. Acad. Sci. USA 104 : 18589 18594.
26. Fuller, R. C. 2002. Lighting environment predicts the relative abundance of male colour morphs in bluefin killifish (Lucania goodei) populations. Proc. R. Soc. Lond. B 269 : 1457 1465.
27. Fuller, R. C., and J. Travis. 2004. Genetics, lighting environment, and heritable responses to lighting environment affect male color morph expression in bluefin killifish, Lucania goodei. Evolution 58 : 1086 1098.
28. Gavrilets, S. 2003. Models of speciation: what have we learned in 40 years? Evolution 57 : 2197 2215.
29. Gavrilets, S. 2004. Fitness landscapes and the origin of species. Monographs in population biology 41. Princeton Univ. Press, Princeton and Oxford.
30. Gavrilets, S., and A. Vose. 2005. Dynamic patterns of adaptive radiation. Proc. Natl. Acad. Sci. USA 102 : 18040 18045.
31. Gavrilets, S., and D. Waxman. 2002. Sympatric speciation by sexual conflict. Proc. Natl Acad. Sci. USA 99 : 10533 10538.
32. Giannini, N. P. 2003. Canonical phylogenetic ordination. Syst. Biol. 52 : 684 695.
33. Gray, S. M., and J. S. McKinnon. 2006. A comparative description of mating behaviour in the endemic telmatherinid fishes of Sulawesi's Malili Lakes. Env. Biol. Fishes 75 : 471 482.
34. Gray, S. M., and J. S. McKinnon. 2007. Linking color polymorphism maintenance and speciation. Trends Ecol. Evol. 22 : 71 79.
35. Gray, S. M., L. M. Dill, F. Y. Tantu, E. R. Loew, F. Herder, and J. S. McKinnon. 2008. Environment contingent sexual selection in a colour polymorphic fish. Proc. R. Soc. Lond. B 275 : 1785 1791.
36. Haffner, G. D., P. E. Hehanussa, and D. Hartoto. 2001. The biology and physical processes of large lakes of Indonesia: lakes Matano and Towuti. Pp. 182 192 in M. Munawar, and R. E. Hecky, eds. The great lakes of the world (GLOW) food web, health and integrity. Backhuis Publishers, Leiden.
37. Herder, F., and J. Freyhof. 2006. Resource partitioning in a tropical stream fish assemblage. J. Fish Biol. 69 : 571 589.
38. Herder F., J. Schwarzer, J. Pfaender, R. K. Hadiaty, and U. K. Schliewen. 2006a. Preliminary checklist of sailfin silversides (Pisces: Telmatherinidae) in the Malili Lakes of Sulawesi (Indonesia), with a synopsis of systematics and threats. Verh. Ges. Ichthyol. 5 : 139 163.
39. Herder, F., A. W. Nolte, J. Pfaender, J. Schwarzer, R. K. Hadiaty, and U. K. Schliewen. 2006b. Adaptive radiation and hybridization in Wallece's Dreamponds: evidence from sailfin silversides in the Malili Lakes of Sulawesi. Proc. R. Soc. Lond. B 273 : 2209 2217.
40. Higashi, M., G. Takimoto, and N. Yamamura. 1999. Sympatric speciation by sexual selection. Nature 402 : 523 526.
41. Kawata, M., A. Shoji, S. Kawamura, and O. Seehausen. 2007. A genetically explicit model of speciation by sensory drive with a continuous population in aquatic environments. BMC Evol. Biol. 7 : 99.
42. Kocher, T. D. 2004. Adaptive evolution and explosive speciation: the cichlid fish model. Nat. Rev. Gen. 5 : 288 298.
43. Kondrashov, A. S., and F. A. Kondrashov. 1999. Interactions among quantitative traits in the course of sympatric speciation. Nature 400 : 351 354.
44. Kottelat, M. 1990a. The ricefish (Oryziidae) of the Malili Lakes, Sulawesi, Indonesia, with description of a new species. Ichthyol. Explor. Freshwaters 1 : 151 166.
45. Kottelat, M. 1990b. Sailfin silversides (Pisces: Telmatherinidae) of Lakes Towuti, Mahalona and Wawontoa (Sulawesi, Indonesia) with descriptions of two new genera and two new species. Ichthyol. Explor. Freshwaters 1 : 227 246.
46. Kottelat, M. 1991. Sailfin silversides (Pisces: Telmatherinidae) of Lake Matano, Sulawesi, Indonesia, with descriptions of six new species. Ichthyol. Explor. Freshwaters 1 : 321 344.
47. Kronforst, M. R., L. G. Young, L. M. Blume, and L. E. Gilbert. 2006. Multilocus analyses of admixture and introgression among hybridizing Heliconius butterflies. Evolution 60 : 1254 1268.
48. Lande, R., O. Seehausen, and J. J. M. van Alphen. 2001. Mechanisms of rapid sympatric speciation by sex reversal and sexual selection in cichlid fish. Genetica 112 : 435 443.
49. Lynch, M., and B. G. Milligan. 1994. Analysis of population genetic structure with RAPD markers. Mol. Ecol. 3 : 91 99.
50. Maan, M. E., O. Seehausen, L. Söderberg, L. Johnson, E. A. P. Ripmeester, H. D. J. Mrosso, M. I. Taylor, T. J. M. van Dooren, and J. J. M. van Alphen. 2004. Intraspecific sexual selection on a speciation trait, male coloration, in the Lake Victoria cichlid Pundamilia nyererei. Proc. R. Soc. Lond. B 271 : 2445 2452.
51. Mallet, J. 1995. A species definition for the modern synthesis. Trends Ecol. Evol. 10 : 294 299.
52. Mallet, J. 2001. The speciation revolution. J. Evol. Biol. 14 : 887 888.
53. Mallet, J. 2005. Hybridization as an invasion of the genome. Trends Ecol. Evol. 20 : 229 237.
54. Mallet, J. 2007. Hybrid speciation. Nature 446 : 279 283.
55. Mayr, E. 1963. Animal species and evolution. Belknap Press, Cambridge, MA.
56. Nei, M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89 : 583 590.
57. Nolte, A. W., and H. D. Sheets. 2005. Shape based assignment tests suggest transgressive phenotypes in natural sculpin hybrids (Teleostei, Scorpaeniformes, Cottidae). Frontiers Zool. 2 : 1 12.
58. Pinkas, L., M. S. Oliphant, and L. K. Iverson. 1971. Food habits of albacore, bluefin tuna and bonito in Californian Waters. Calif. Fish Game 152 : 1 105.
59. ST in three-spined stickleback (Gasterosteus aculeatus) populations along a coastal-inland gradient. Mol. Ecol. 16 : 891 905.
60. Rogers, S. M., and L. Bernatchez. 2005. Integrating QTL mapping and genome scans towards the characterization of candidate loci under parallel selection in the lake whitefish (Coregonus clupeaformis). Mol. Ecol. 14 : 351 361.
61. Rolán-Alvarez, E. 2007. Sympatric speciation as a by-product of ecological adaptation in the Galician Littorina saxatilis hybrid zone. J. Moll. Stud. 73 : 1 10.
62. Roy, D., M. F. Docker, P. Hehanussa, D. D. Heath, and G. D. Haffner. 2004. Genetic and morphological data supporting the hypothesis of adaptive radiation in the endemic fish of Lake Matano. J. Evol. Biol. 17 : 1268 1276.
63. Roy, D., M. F. Docker, G. D. Haffner, and D. D. Heath. 2007a. Body shape vs. colour associated initial divergence in the Telmatherina radiation in Lake Matano, Sulawesi, Indonesia. J. Evol. Biol. 20 : 1126 1137.
64. Roy, D., M. F. Docker, G. Paterson, P. B. Hamilton, D. D. Heath, and G. D. Haffner. 2007b. Resource-based adaptive divergence in the freshwater fish Telmatherina from Lake Matano, Indonesia. Mol. Ecol. 16 : 35 48.
65. Savolainen, V., M.-C. Anstett, C. Lexer, I. Hutton, J. J. Clarkson, M. V. Norup, M. P. Powell, D. Springate, N. Salamin, and W. J. Baker. 2006. Sympatric speciation in palms on an oceanic island. Nature 441 : 210 213.
66. Schliewen, U. K., and B. Klee. 2004. Reticulate sympatric speciation in Cameroonian crater lake cichlids. Front. Zool. 1 : 1 12.
67. Schliewen, U. K., D. Tautz, and S. Pääbo. 1994. Sympatric speciation suggested by monophyly of crater lake cichlids. Nature 368 : 629 632.
68. Schliewen, U. K., K. Rassmann, M. Markmann, J. Markert, T. Kocher, and D. Tautz. 2001. Genetic and ecological divergence of a monophyletic cichlid species pair under fully sympatric conditions in Lake Ejagham, Cameroon. Mol. Ecol. 10 : 1471 1488.
69. Schoener, T. W. 1970. Nonsynchronous spatial overlap of lizards in patchy habitats. Ecology 51 : 408 418.
70. Seehausen, O. 2004. Hybridization and adaptive radiation. Trends Ecol. Evol. 19 : 198 207.
71. Seehausen, O., and J. J. M. van Alphen. 1998. The effect of male coloration on female mate choice in closely related Lake Victoria cichlids (Haplochromis nyererei complex). Behav. Ecol. Sociobiol. 42 : 1 8.
72. Takimoto, G., M. Higashi, and N. Yamamura. 2000. A deterministic genetic model for sympatric speciation by sexual selection. Evolution 54 : 1870 1881.
73. Templeton, A. R. 1981. Mechanisms of speciation - a population genetic approach. Annu. Rev. Ecol. Syst. 12 : 23 48.
74. ter Braak, C. J. F., and P. Smilauer. 1998. CANOCO reference manual and users guide to Canoco for Windows. 351. Centre for Biometry, Wageningen.
75. Turelli, M., N. H. Barton, and J. A. Coyne. 2001. Theory and speciation. Trends Ecol. Evol. 16 : 330 343.
76. Turner, G. F., and M. T. Burrows. 1995. A model of sympatric speciation by sexual selection. Proc. R. Soc. Lond. B 260 : 287 292.
77. Vekemans, X. 2002. AFLP-SURV version 1.0. Distributed by the author. Université Libre, Laboratoire Génétique et Ecologie Végétale, Bruxelles.
78. Via, S. 2001. Sympatric speciation in animals: the ugly duckling grows up. Trends Ecol. Evol. 16 : 381 390.
79. von Rintelen, T., A. B. Wilson, A. Meyer, and M. Glaubrecht. 2004. Escalation and trophic specialization drive adaptive radiation of freshwater gastropods in ancient lakes on Sulawesi, Indonesia. Proc. R. Soc. Lond. B 271 : 2541 2549.
80. von Rintelen, T., P. Bouchet, and 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.
81. Vos, P., R. Hogers, M. Bleeker, M. Reijans, T. van de Lee, M. Hornes, A. Frijters, J. Pot, J. Peleman, M. Kuiper, and M. Zabeau. 1995. AFLP: a new technique for DNA fingerprinting. Nucl. Acids Res. 23 : 4407 4414.
82. Wright, S. 1943. Isolation by distance. Genetics 28 : 114 138.
83. Wright, S. 1946. Isolation by distance under diverse systems of mating. Genetics 31 : 39 59.
84. Wu, C.-I. 2001. The genic view of the process of speciation. J. Evol. Biol. 14 : 851 865.
85. Zelditch, M. L., D. L. Swiderski, H. D. Sheets, and W. L. Fink. 2004. Geometric morphometrics for biologists. Academic Press, London. U.K.