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Genetic linkage of ecological specialization and reproductive isolation in pea aphids

Abstract

The evolution of ecological specialization generates biological diversity and may lead to speciation1,2,3. Genetic architecture can either speed or retard this process. If resource use and mate choice have a common genetic basis through pleiotropy or close linkage, the resulting genetic correlations can promote the joint evolution of specialization and reproductive isolation, facilitating speciation4,5,6. Here we present a model of the role of genetic correlations in specialization and speciation, and test it by analysing the genetic architecture of key traits in two highly specialized host races of the pea aphid (Acyrthosiphon pisum pisum; Hemiptera : Aphididae). We found several complexes of pleiotropic or closely linked quantitative trait loci (QTL) that affect key traits in ways that would promote speciation: QTL with antagonistic effects on performance on the two hosts are linked to QTL that produce asortative mating (through habitat choice). This type of genetic architecture may be common in taxa that have speciated under divergent natural selection.

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Figure 1: Network of complementary genetic correlations affecting specialization and speciation.
Figure 2: Linkage map of pea aphid, with quantitative trait loci (QTL) for ecological specialization and reproductive isolation.

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References

  1. Thompson, J. N. The Coevolutionary Process (Univ. Chicago Press, Chicago, 1994).

    Book  Google Scholar 

  2. Schluter, D. in Endless Forms: Species and Speciation (eds Howard, D. J. & Berlocher, S. H.) 114–129 (Oxford Univ. Press, New York, 1998).

    Google Scholar 

  3. Futuyma, D. J. & Moreno, G. The evolution of ecological specialization. Annu. Rev. Ecol. Syst. 19, 201–233 (1988).

    Article  Google Scholar 

  4. Felsenstein, J. Skepticism toward Santa Rosalia, or why are there so few kinds of animals? Evolution 35, 124–138 (1981).

    Article  PubMed  Google Scholar 

  5. Kondrashov, A. S. & Mina, M. V. Sympatric speciation, when is it possible? Biol. J. Linn. Soc. 27, 201–233 (1986).

    Article  Google Scholar 

  6. Rice, W. R. Selection via habitat specialization, the evolution of reproductive isolation as a correlated character. Evol. Ecol. 1, 301–314 (1987).

    Article  Google Scholar 

  7. Schemske, D. W. Understanding the origin of species. Evolution 54, 1069–1073 (2000).

    Article  Google Scholar 

  8. Lande, R. Quantitative genetic analysis of multivariate evolution, applied to brain: body size allometry. Evolution 33, 402–416 (1979).

    Article  PubMed  Google Scholar 

  9. Orr, H. A. The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics 139, 1805–1813 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Fry, J. D. The evolution of host specialization, are trade-offs overrated? Am. Nat. 148, S84–S107 (1996).

    Article  Google Scholar 

  11. Via, S. The genetic structure of host plant adaptation in a spatial patchwork: demographic variability among reciprocally transplanted pea aphid clones. Evolution 45, 827–852 (1991).

    Article  PubMed  Google Scholar 

  12. Filchak, K. E., Roethele, J. B. & Feder, J. L. Natural selection and sympatric divergence in the apple maggot Rhagoletis pomonella. Nature 407, 739–742 (2000).

    Article  CAS  PubMed  Google Scholar 

  13. Bush, G. L. Sympatric speciation in animals: new wine in old bottles. Trends Ecol. Evol. 9, 285–288 (1994).

    Article  CAS  PubMed  Google Scholar 

  14. Rice, W. R. & Hostert, E. Laboratory experiments on speciation. What have we learned in 40 years? Evolution 47, 1637–1653 (1993).

    Article  PubMed  Google Scholar 

  15. Via, S. & Lande, R. Genotype–environment interaction and the evolution of phenotypic plasticity. Evolution 39, 505–522 (1985).

    Article  PubMed  Google Scholar 

  16. Eastop, V. F. Keys for the identification of Acyrthosiphon (Hemiptera : Aphididae). Bull. Br. Mus. Nat. Hist. B 26, 1–115 (1973).

    Google Scholar 

  17. Via, S. Reproductive isolation between sympatric races of pea aphids. I. Gene flow restriction and habitat choice. Evolution 53, 1446–1457 (1999).

    Article  PubMed  Google Scholar 

  18. Via, S., Bouck, A. C. & Skillman, S. Reproductive isolation between sympatric races of pea aphids. II. Selection against migrants and hybrids in the parental environments. Evolution 54, 1626–1637 (2000).

    Article  CAS  PubMed  Google Scholar 

  19. Lande, R. The genetic correlation between characters maintained by selection, linkage and inbreeding. Genet. Res. Cambridge 44, 309–320 (1984).

    Article  CAS  Google Scholar 

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

    Google Scholar 

  21. Sun, R. Y. & Robinson, A. G. Chromosome studies of 50 species of aphids. Can. J. Zool. 44, 649–653 (1966).

    Article  CAS  PubMed  Google Scholar 

  22. Orr, H. A. Testing natural selection vs. genetic drift in phenotypic evolution using quantitative trait locus data. Genetics 149, 2099–2104 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Caillaud, C. M. & Via, S. Specialized feeding behavior influences both ecological specialization and assortative mating in sympatric host races of pea aphids. Am. Nat. 156, 609–621 (2000).

    Article  Google Scholar 

  24. Whitlock, M. C. The Red Queen beats the jack-of-all-trades? The limitations on the evolution of phenotypic plasticity and niche breadth. Am. Nat. 148, S65–S77 (1996).

    Article  Google Scholar 

  25. Via, S. Sympatric speciation in animals: the ugly duckling grows up. Trends Ecol. Evol. 16, 381–390 (2001).

    Article  CAS  PubMed  Google Scholar 

  26. Lander, E. S. et al. MAPMAKER, an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1, 174–181 (1987).

    Article  CAS  PubMed  Google Scholar 

  27. Cho, Y. G. et al. Cloning and mapping of variety specific rice genomic DNA sequences: Amplified fragment length polymorphisms (AFLP) from silver stained polyacrylamide gels. Genome 39, 373–378 (1996).

    Article  CAS  PubMed  Google Scholar 

  28. Littel, R. C. et al. SAS System for Mixed Models (SAS Institute, Cary, North Carolina, 1996).

    Google Scholar 

  29. Basten, C. J., Weir, B. S. & Zeng, Z.-B. QTL Cartographer (Version 1.13) (Department of Statistics, North Carolina State University, Raleigh, North Carolina, 1996).

  30. Churchill, G. & Doerge, R. W. Empirical threshold values for quantitative trait locus mapping. Genetics 138, 963–971 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank G. Churchill, D. Schemske, D. Schluter and Z.-B. Zeng for discussions. M. Arnold, T. Bradshaw, J. Conner, K. Shaw and J. Wilkinson provided useful comments on the manuscript. Z.-B. Zeng provided the calculation from ref. 22, and R. Lande pointed out the effects of cyclical parthenogenesis on recombination rates. A. Bouck, S. Skillman, C. Olson and A. Badgley provided expert technical assistance. This work was supported by NSF and USDA grants to S.V. and D.J.H.

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Correspondence to Sara Via.

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Hawthorne, D., Via, S. Genetic linkage of ecological specialization and reproductive isolation in pea aphids. Nature 412, 904–907 (2001). https://doi.org/10.1038/35091062

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