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The genetic architecture of divergence between threespine stickleback species

Naturevolume 414, pages901–905 (2001)Cite this article

Abstract

The genetic and molecular basis of morphological evolution is poorly understood, particularly in vertebrates. Genetic studies of the differences between naturally occurring vertebrate species have been limited by the expense and difficulty of raising large numbers of animals and the absence of molecular linkage maps for all but a handful of laboratory and domesticated animals. We have developed a genome-wide linkage map for the three-spined stickleback (Gasterosteus aculeatus), an extensively studied teleost fish that has undergone rapid divergence and speciation since the melting of glaciers 15,000 years ago1. Here we use this map to analyse the genetic basis of recently evolved changes in skeletal armour and feeding morphologies seen in the benthic and limnetic stickleback species from Priest Lake, British Columbia. Substantial alterations in spine length, armour plate number, and gill raker number are controlled by genetic factors that map to independent chromosome regions. Further study of these regions will help to define the number and type of genetic changes that underlie morphological diversification during vertebrate evolution.

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Figure 1: Representative benthic and limnetic fish from Priest Lake, British Columbia, are stained with alizarin red to highlight bone.
Figure 2: Genetic linkage map ofGasterosteus aculeatus.
Figure 3: Mapping of morphological traits in the Priest Lake cross.

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References

  1. Bell, M. A. & Foster, S. A.The Evolutionary Biology of the Threespine Stickleback (Oxford Science, New York, 1994).

    Google Scholar 

  2. McPhail, J. D. inThe Evolutionary Biology of the Threespine Stickleback (eds Bell, M. A. & Foster, S. A.) 399–437 (Oxford Univ. Press, New York, 1994).

    Google Scholar 

  3. Ridgway, M. S. & McPhail, J. D. Ecology and evolution of sympatric sticklebacks (Gasterosteus): mate choice and reproductive isolation in the Enos Lake species pair.Can. J. Zool.62, 1813–1818 (1984).

    Article  Google Scholar 

  4. Nagel, L. & Schluter, D. Body size, natural selection, and speciation in sticklebacks.Evolution52, 209–218 (1998).

    Article  Google Scholar 

  5. Hatfield, T. & Schluter, D. Ecological speciation in sticklebacks: environment-dependent hybrid fitness.Evolution53, 866–873 (1999).

    Article  Google Scholar 

  6. Vamosi, S. M. & Schluter, D. Sexual selection against hybrids between sympatric stickleback species: evidence from a field experiment.Evolution53, 874–879 (1999).

    Article  Google Scholar 

  7. Rico, C., Zadworny, D., Kuhnlein, U. & Fitzgerald, G. J. Characterization of hypervariable microsatellite loci in the threespine sticklebackGasterosteus aculeatus.Mol. Ecol.7, 271–272 (1993).

    Article  Google Scholar 

  8. Taylor, E. B. Microsatellites isolated from the threespine sticklebackGasterosteus aculeatus.Mol. Ecol.7, 925–931 (1998).

    Article CAS  Google Scholar 

  9. Largiader, C. R., Fries, V., Kobler, B. & Bakker, C. M. Isolation and characterization of microsatellite loci from the three-spined stickleback (Gasterosteus aculeatus L.).Mol. Ecol.8, 342–344 (1999).

    CAS PubMed  Google Scholar 

  10. Stam, P. & Van Ooijen . JoinMap, version 2.0: Software for the calculation of genetic linkage maps. (Centre for Plant Breeding and Reproduction Research, Wageningen, 1995).

  11. Chen, T.-R. & Reisman, H. M. A comparative study of the North American species of sticklebacks (Teleostei: Gasterosteidae).Cytogenetics9, 321–332 (1970).

    Article CAS  Google Scholar 

  12. Bentzen, P. & McPhail, J. D. Ecology and evolution of sympatric sticklebacks (Gasterosteus): specialization for alternative trophic niches in the Enos Lake species pair.Can. J. Zool.62, 2280–2286 (1984).

    Article  Google Scholar 

  13. Schluter, D. Adaptive radiation in sticklebacks: size, shape, and habitat use efficiency.Ecology74, 699–709 (1993).

    Article  Google Scholar 

  14. Hatfield, T. Genetic divergence in adaptive characters between sympatric species of stickleback.Am. Nat.149, 1009–1029 (1997).

    Article CAS  Google Scholar 

  15. Hagen, D. W. & Gilbertson, L. G. Geographic variation and environmental selection inGasterosteus aculeatus L. in the Pacific Northwest, America.Evolution26, 32–51 (1972).

    Article CAS  Google Scholar 

  16. Moodie, G. E. E. Predation, natural selection and adaptation in an unusual threespine stickleback.Heredity28, 155–167 (1972).

    Article  Google Scholar 

  17. Reimchen, T. E. Spine deficiency and polymorphism in a population of (Gasterosteus aculeatus): an adaptation to predators?Can. J. Zool.58, 1232–1244 (1980).

    Article  Google Scholar 

  18. Reimchen, T. E. Structural relationship between spines and lateral plates in threespine stickleback (Gasterosteus aculeatus).Evolution37, 931–946 (1983).

    CAS PubMed  Google Scholar 

  19. Hawthorne, D. J. & Via, S. Genetic linkage of ecological specialization and reproductive isolation in pea aphids.Nature412, 904–907 (2001).

    Article ADS CAS  Google Scholar 

  20. Lynch, M. & Walsh, J. B.Genetics and Analysis of Quantitative Traits (Sinauer, Massachusetts, 1998).

    Google Scholar 

  21. Ahn, D. & Gibson, G. Axial variation in the threespine stickleback: genetic and environmental factors.Evol. Dev.1, 100–112 (1999).

    Article CAS  Google Scholar 

  22. Reimchen, T. E. Predator-induced cyclical changes in lateral plate frequencies ofGasterosteus.Behavior132, 1079–1094 (1995).

    Article  Google Scholar 

  23. Swain, D. P. Selective predation for vertebral phenotype inGasterosteus aculeatus: reversal in the direction of selection at different larval sizes.Evolution46, 998–1013 (1992).

    PubMed  Google Scholar 

  24. Orr, H. A. The genetics of species differences.Trends Ecol. Evol.16, 343–350 (2001).

    Article  Google Scholar 

  25. Beavis, W. D. inMolecular Dissection of Complex Traits (ed. Paterson, A. H.) 145–162 (CRC Press, Boca Raton, 1998).

    Google Scholar 

  26. Hinegardner, R. Evolution of cellular DNA content in teleost fishes.Am. Nat.102, 517–523 (1968).

    Article  Google Scholar 

  27. Rozen, S. & Skaletsky, H. J. Primer3; code available athttp://www-genome.wi.mit.edu/ genome_software/other/primer3.html (1997).

  28. VanOoijen, J. W. & Maliepard, C. MapQTL, version 3.0: Software for the calculation of QTL positions on genetic maps. (Centre for Plant Breeding and Reproduction Research, Wageningen, 1996).

  29. VanOoijen, J. W. LOD significance thresholds for QTL analysis in experimental populations of diploid species.Heredity83, 613–624 (1999).

    Article  Google Scholar 

  30. Bell, M. A. inEvolutionary Genetics of Fishes (ed. Turner, B. J.) 431–528 (Plenum, New York, 1984).

    Book  Google Scholar 

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Acknowledgements

We thank S. Anderson, R. Melzer, K. Tsui, C. Uhlick and R. Vega for technical assistance. D.S. was supported by a Natural Sciences and Engineering Research Council of Canada research grant. C.L.P. is a research associate and D.M.K. is an assistant investigator of the Howard Hughes Medical Institute.

Author information

Authors and Affiliations

  1. Department of Developmental Biology and Howard Hughes Medical Institute, Stanford University, Stanford, 94305-5329, California, USA

    Catherine L. Peichel, Kirsten S. Nereng, Kenneth A. Ohgi, Bonnie L. E. Cole, Pamela F. Colosimo & David M. Kingsley

  2. Department of Biology, University of Wisconsin-Eau Claire, Eau Claire, 54702-4004, Wisconsin, USA

    C. Alex Buerkle

  3. Zoology Department and Centre for Biodiversity, University of British Columbia, Vancouver, V6T 1ZT, British Columbia, Canada

    Dolph Schluter

Authors
  1. Catherine L. Peichel
  2. Kirsten S. Nereng
  3. Kenneth A. Ohgi
  4. Bonnie L. E. Cole
  5. Pamela F. Colosimo
  6. C. Alex Buerkle
  7. Dolph Schluter
  8. David M. Kingsley

Corresponding author

Correspondence toDavid M. Kingsley.

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Competing interests

The authors declare no competing financial interests.

Supplementary information

41586_2001_BF414901a_MOESM1_ESM.doc

Supplementary Table: Phenotype means of fish with different allele combinations at most closely linked microsatellite (DOC 26 kb)

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Peichel, C., Nereng, K., Ohgi, K.et al. The genetic architecture of divergence between threespine stickleback species.Nature414, 901–905 (2001). https://doi.org/10.1038/414901a

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