Advertisement

Naturwissenschaften

, Volume 95, Issue 12, pp 1175–1180 | Cite as

Divergent evolution of feeding substrate preferences in a phylogenetically young species flock of pupfish (Cyprinodon spp.)

  • Joachim Horstkotte
  • Martin Plath
Short Communication

Abstract

A fundamental question in sympatric speciation is how trophic divergence is achieved. We used an extremely young (<8,000 years) species flock of pupfish (Cyprinodon spp.) from Laguna Chichancanab in south-eastern Mexico to examine divergent evolution of preferences for different feeding substrates. In a test aquarium, we presented four feeding substrates (sand, gravel, a plastic plant, and blank bottom), but no actual food was offered. The four feeding substrates were chosen to mirror the most common substrate types in Laguna Chichancanab. Previous studies demonstrated that benthic food items prevail in the diet of most Cyprinodon species. C. beltrani preferred sand, whereas C. labiosus preferred gravel. F1 hybrids of both species showed intermediate preferences. C. maya searched for food equally at all substrates. As the test fish were reared under identical laboratory conditions (i.e., in the absence of feeding substrates), the species-specific preferences appear to be genetically fixed, suggesting rapid divergent evolution of feeding behaviors.

Keywords

Sympatric speciation Trophic segregation Niche partitioning Foraging behavior Habitat choice 

Notes

Acknowledgment

We thank H. Wilkens and U. Strecker for providing the fish. T. Czeschlik and two anonymous reviewers provided very constructive comments. M. Hänel prepared the drawings of the fish. The experiments reported in this paper comply with the current laws of Germany.

References

  1. Arnegard ME, Kondrashov AS (2004) Sympatric speciation by sexual selection alone is unlikely. Evolution 58:222–237PubMedGoogle Scholar
  2. Barluenga M, Stolting KN, Salzburger W, Muschick M, Meyer A (2006) Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature 439:719–723PubMedCrossRefGoogle Scholar
  3. Boughman JW, Rundle HD, Schluter D (2005) Parallel evolution of sexual isolation in sticklebacks. Evolution 59:361–373PubMedGoogle Scholar
  4. Bouton N, Seehausen O, van Alphen JJM (1997) Resource partitioning among rock dwelling haplochromines (Pisces: Cichlidae) from Lake Victoria. Ecol Freshw Fish 6:225–240CrossRefGoogle Scholar
  5. Carballo M, Carballero A, Rolán-Alvarez E (2005) Habitat-dependent ecotype microdistribution at the midshore in natural populations of Littorina saxatilis. Hydrobiologia 548:307–311CrossRefGoogle Scholar
  6. Couldridge VCK, Alexander GJ (2002) Color patterns and species recognition in four closely related species of Lake Malawi cichlid. Behav Ecol 13:59–64CrossRefGoogle Scholar
  7. Covich A, Stuiver M (1974) Changes in oxygen 18 as a measure of long-term fluctuations in tropical lake levels and molluscan populations. Limnol Ocean 19:682–691CrossRefGoogle Scholar
  8. Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland, MAGoogle Scholar
  9. Cruz R, Carballo P, Conde-Padín P, Rolán-Alvarez E (2004) Testing alternative models for sexual isolation in natural populations of Littorina saxatilis: indirect support for by-product ecological speciation? J Evol Biol 17:288–293PubMedCrossRefGoogle Scholar
  10. Diekmann U, Doebeli M (1999) On the origin of species by sympatric speciation. Nature 400:354–357CrossRefGoogle Scholar
  11. Doebeli M, Diekmann U (2000) Evolutionary branching and sympatric speciation caused by different types of ecological interactions. Am Nat 156:S77–S101CrossRefGoogle Scholar
  12. Echelle AA, Carson EW, Echelle AF, Van den Busche RA, Dowling TE, Meyer A (2005) Historical biogeography of the New World pupfish genus Cyprinodon (Teleostei, Cyprinodontidae). Copeia 2005:220–239CrossRefGoogle Scholar
  13. Erlandsson J, Rolán-Alvarez E, Johannesson K (1998) Migratory differences between ecotypes of the snail Littorina saxatilis on the Galician rocky shores. Evol Ecol 12:913–924CrossRefGoogle Scholar
  14. Feulner PGD, Kirschbaum F, Mamonekene V, Ketmaier V, Tiedemann R (2007) Adaptive radiation in African weakly electric fish (Teleostei: Mormyridae: Campylomormyrus): a combined molecular and morphological approach. J Evol Biol 20:403–414PubMedCrossRefGoogle Scholar
  15. Goldschmidt T, Witte F, de Visser J (1990) Ecological segregation in zooplanktivorous haplochromine cichlids (Pisces, Cichlidae) from Lake Victoria. Oikos 58:343–355CrossRefGoogle Scholar
  16. Greenwood PH (1984) What is a species flock? In: Echelle AA, Kornfield I (eds) Evolution of fish species flocks. University of Maine at Orono Press, Orono, pp 13–19Google Scholar
  17. Hodell DA, Brenner M, Curtis JH, Guilderson T (2001) Solar forcing of drought frequency in the Maya lowlands. Science 292:1367–1370PubMedCrossRefGoogle Scholar
  18. Hollander J, Lindegarth M, Johannesson K (2005) Local adaptation but not geographical separation promotes assortative mating in a snail. Anim Behav 70:1208–1219CrossRefGoogle Scholar
  19. Holtmeier CL (2001) Heterochrony, maternal effects, and phenotype variation among sympatric pupfishes. Evolution 55:330–338PubMedGoogle Scholar
  20. Horstkotte J (2005) Trophische Anpassungen innerhalb des Cyprinodon-Artenschwarmes (Cyprinodontidae, Teleostei) aus der Laguna Chichancanab (Mexiko). Z Fischk Suppl 3:1–92Google Scholar
  21. Horstkotte J, Strecker U (2005) Trophic differentiation in the phylogenetically young Cyprinodon species flock (Cyprinodontidae Teleostei) from Laguna Chichancanab (Mexico). Biol J Linn Soc 85:125–134CrossRefGoogle Scholar
  22. Humphries JM (1984a) Cyprinodon verecundus, n. sp., a fifth species of pupfish from Laguna Chichancanab. Copeia 1984:58–68CrossRefGoogle Scholar
  23. Humphries JM (1984b) Genetics of speciation in pupfishes from Laguna Chichancanab, Mexico. In: Echelle AA, Kornfield I (eds) Evolution of fish species flocks. University of Maine at Orono Press, Orono, pp 129–139Google Scholar
  24. Humphries JM, Miller RR (1981) A remarkable species flock of pupfishes genus Cyprinodon from Yucatan, Mexico. Copeia 1981:52–64CrossRefGoogle Scholar
  25. Johannesson K (2001) Parallel speciation: a key to sympatric divergence. Trends Ecol Evol 16:148–153PubMedCrossRefGoogle Scholar
  26. Johannesson K, Rolán-Alvarez E, Ekendahl E (1995) Incipient reproductive isolation between two sympatric morphs of the intertidal snail Littorina saxatilis. Evolution 49:1180–1190CrossRefGoogle Scholar
  27. Johnson TC, Scholz CA, Talbot MR, Kelts K, Ricketts RD, Ngobi G, Beuning K, Ssemanda I, McGill JW (1996) Late Pleistocene dessication of Lake Victoria and rapid evolution of cichlid fishes. Science 273:1091–1093PubMedCrossRefGoogle Scholar
  28. Mayr E (1942) Systematics and the origin of species. Colombia University Press, New YorkGoogle Scholar
  29. McKaye KR (1980) Seasonality in habitat selection by the gold color morph of Cichlasoma citrinellum and its relevance to sympatric speciation in the family Cichlidae. Environ Biol Fish 5:75–78CrossRefGoogle Scholar
  30. McKinnon JS, Mori S, Blackman BK, David L, Kingsley DM, Jamieson L, Chou J, Schluter D (2004) Evidence for ecology’s role in speciation. Nature 429:294–298PubMedCrossRefGoogle Scholar
  31. McPhail JD (1992) Ecology and evolution of sympatric sticklebacks (Gasterosteus): evidence for a species-pair in Paxton Lake, Texas Island, British Columbia. Can J Zool 70:361–369CrossRefGoogle Scholar
  32. Meyer A, Kocher TD, Basasibwaki P, Wilson AC (1990) Monophyletic origin of Lake Victoria cichlid fishes suggested by mitochondrial DNA sequences. Nature 347:550–553PubMedCrossRefGoogle Scholar
  33. Nagel L, Schluter D (1998) Body size, natural selection, and speciation in sticklebacks. Evolution 52:209–218CrossRefGoogle Scholar
  34. Nagl S, Tichy H, Mayer WE, Takezaki N, Takehata N, Klein J (2000) The origin and age of haplochromine fishes in Lake Victoria, East Africa. Proc R Soc Lond B 267:1049–1061CrossRefGoogle Scholar
  35. Plath M, Strecker U (2008) Behavioral diversification in a young species flock of pupfish (Cyprinodon spp. Cyprinodontidae Teleostei): shoaling and aggressive behavior. Behav Ecol Sociobiol (in press)Google Scholar
  36. Quesada H, Posada D, Caballero A, Morán P, Rolán-Alvarez E (2007) Phylogenetic evidence for multiple sympatric ecological diversification in a marine snail. Evolution 61:1600–1612PubMedCrossRefGoogle Scholar
  37. Ribbink AJ (1984) Is the species flock concept tenable? In: Echelle AA, Kornfield I (eds) Evolution of fish species flocks. University of Maine at Orono, Orono, pp 21–25Google Scholar
  38. Rolán-Alvarez E, Johannesson K, Erlandsson J (1997) The maintenance of a cline in the marine snail Littorina saxatilis: the role of home site advantage and hybrid fitness. Evolution 51:1838–1847CrossRefGoogle Scholar
  39. Rosenzweig ML (1995) Species diversity in space and time. Cambridge University Press, Cambridge, p 436Google Scholar
  40. Savolainen V, Anstett M-C, Lexer C, Hutton I, Clarkson JJ, Norup MV, Powell MP, Springate MP, Salamin N, Baker WJ (2006) Sympatric speciation in palms on an oceanic island. Nature 441:210–213PubMedCrossRefGoogle Scholar
  41. Schliewen UK, Tautz D, Pääbo S (1994) Sympatric speciation suggested by monophyly of crater lake cichlids. Nature 368:629–632PubMedCrossRefGoogle Scholar
  42. Schliewen UK, Kocher TD, McKaye KR, Seehausen O, Tautz D (2006) Evidence for sympatric speciation? Science 444:E12–E13Google Scholar
  43. Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, OxfordGoogle Scholar
  44. Schluter D (2001) Ecology and the origin of species. Trends Ecol Evol 16:372–380PubMedCrossRefGoogle Scholar
  45. Seehausen O, Alphen JJM, Witte F (1997) Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277:1808–1811CrossRefGoogle Scholar
  46. Soltz DL, Naiman RJ (1978) The natural history of native fishes in the Death Valley system. Nat Hist Mus Los Angeles Cty Sci Ser 30:75Google Scholar
  47. Stevenson MM (1992) Food habits within the Laguna Chichancanab Cyprinodon (Pisces: Cyprinodontidae) species flock. Southw Nat 37:337–343CrossRefGoogle Scholar
  48. Strecker U (1996) Molekulargenetische und ethologische Untersuchungen zur Speziation eines Artenschwarmes der Gattung Cyprinodon (Cyprinodontidae, Teleostei). PhD thesis, Universität HamburgGoogle Scholar
  49. Strecker U (2002) Cyprinodon esconditius, a new pupfish from Laguna Chichancanab, Yucatan, Mexico (Cyprinodontidae). Cybium 26:301–307Google Scholar
  50. Strecker U (2004) The Cyprinodon species flock from Laguna Chichancanab, Mexico (Teleostei): sexual and disruptive selection driving adaptive radiation. Mitteil Hamb Zool Mus Inst 101:65–74Google Scholar
  51. Strecker U (2005) Description of a new species from Laguna Chichancanab, Yucatan, Mexico: Cyprinodon suavium (Pisces: Cyprinodontidae). Hydrobiologia 541:107–115CrossRefGoogle Scholar
  52. Strecker U (2006a) Genetic differentiation and reproductive isolation in a Cyprinodon fish species flock from Laguna Chichancanab, Mexico. Mol Phylogenet Evol 39:865–872PubMedCrossRefGoogle Scholar
  53. Strecker U (2006b) The impact of invasive fish on an endemic Cyprinodon species flock (Teleostei) from Laguna Chichancanab, Yucatan, Mexico. Ecol Freshw Fish 15:408–418CrossRefGoogle Scholar
  54. Strecker U, Kodric-Brown A (1999) Mate recognition systems in a species flock of Mexican pupfish. J Evol Biol 12:927–935CrossRefGoogle Scholar
  55. Strecker U, Meyer CG, Sturmbauer C, Wilkens H (1996) Genetic divergence and speciation in an extremely young species flock in Mexico formed by the genus Cyprinodon (Cyprinodontidae Teleostei). Mol Phylogenet Evol 6:143–149PubMedCrossRefGoogle Scholar
  56. Sturmbauer C, Meyer CG (1992) Genetic divergence, speciation and morphological stasis in a lineage of African cichlid fishes. Nature 358:578–581PubMedCrossRefGoogle Scholar
  57. Tobler M, Schlupp I, Heubel KU, Riesch R, García de León FJ, Giere O, Plath M (2006) Life on the edge: Hydrogen sulfide and the fish communities of a Mexican cave and surrounding waters. Extremophiles 10(6):577–585PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.Biozentrum Grindel and Zoological MuseumUniversität HamburgHamburgGermany
  2. 2.Universität Potsdam, Institut für Biochemie/Biologie, Abteilung für Evolutionsbiologie/Spezielle ZoologiePotsdamGermany
  3. 3.Universität Potsdam, Institut für Biochemie/Biologie, Abteilung für TierökologiePotsdamGermany

Personalised recommendations