Skip to main content
SpringerLink
Log in

Recombination and the Divergence of Hybridizing Species

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

The interplay between hybridization and recombination can have a dramatic effect on the likelihood of speciation or persistence of incompletely isolated species. Many models have suggested recombination can oppose speciation, and several recent empirical investigations suggest that reductions in recombination between various components of reproductive isolation and/or adaptation can allow species to persist in the presence of gene flow. In this article, we discuss these ideas in relation to speciation models, phylogenetic analyses, and species concepts. In particular, we revisit genetic architectures and population mechanisms that create genetic correlations and facilitate divergence in the face of gene flow. Linkage among genes contributing to adaptation or reproductive isolation due to chromosomal rearrangements as well as pleiotropy or proximity of loci can greatly increase the odds of species divergence or persistence. Finally, we recommend recombination to be a focus of inquiry when studying the origins of biological diversity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Anderson, W.W., T. Dobzhansky, O. Pavlovsky, J.R. Powell & D. Yardley, 1975. Three decades of genetic change in Drosophila pseudoobscura. Evolution 29: 24–36.

    Google Scholar 

  • Anderson, W.W., J. Arnold, D.G. Baldwin, A.T. Beckenbach, C.J. Brown, S.H. Bryant, J.A. Coyne, L.G. Harshman, W.B. Heed, D.E. Jeffery, L.B. Klaczko, B.C. Moore, J.M. Porter, J.R. Powell, T. Prout, S.W. Schaeffer, J.C. Stephens, C.E. Taylor, M.E. Turner, G.O. Williams & J.A. Moore, 1991. Four decades of inversion polymorphism in Drosophila pseudoobscura. P. Natl. Acad. Sci. USA 88: 10367–10371.

    Google Scholar 

  • Aquadro, C.F., A.L. Weaver, S.W. Schaeffer & W.W. Anderson, 1991. Molecular evolution of inversions in Drosophila pseudoobscura: the amylase gene region. P. Natl. Acad. Sci. USA 88: 305–309.

    Google Scholar 

  • Ballard, J.W., 2000. When one is not enough: introgression of mitochondrial DNA in Drosophila. Mol. Biol. Evol. 17: 1126–1130.

    Google Scholar 

  • Barton, N.H. & B.O. Bengtsson, 1986. The barrier to genetic exchange between hybridizing population. Heredity 56: 357–376.

    Google Scholar 

  • Barton, N.H.& G.M. Hewitt, 1985. Analysis of hybrid zones. Annu. Rev. Ecol. Syst. 16: 113–148.

    Google Scholar 

  • Barton, N.H. & M. Turelli, 1991. Natural and sexual selection on many loci. Genetics 127: 229–255.

    Google Scholar 

  • Berlocher, S.H. & J.L. Feder, 2002. Sympatric speciation in phytophagous insects: moving beyond the controversy? Annu. Rev. Entomol. 47: 773–815.

    Google Scholar 

  • Brooks, R., 2000. Negative genetic correlation between male sexual attractiveness and survival. Nature 406: 67–70.

    Google Scholar 

  • Carpenter, A.T.C., 1979. Synaptonemal complex and recombination nodules in wild-type Drosophila melanogaster females. Genetics 92: 511–541.

    Google Scholar 

  • Carson, H.L., 1975. The genetics of speciation at the diploid level. Am. Nat., 109: 83–92.

    Google Scholar 

  • Diehl, S.R. & G.L. Bush, 1989. The Role of Habitat Preference in Adaptation and Speciation. Sinauer Press, Sunderland, Massachusetts.

    Google Scholar 

  • Dobzhansky, T., 1951. Genetics and the Origin of Species. Columbia University Press, New York.

    Google Scholar 

  • Dobzhansky, T., 1973. Is there gene exchange between Drosophila pseudoobscura and Drosophila persimilis in their natural habitats? Am. Nat., 107: 312–314.

    Google Scholar 

  • Felsenstein, J., 1981. Skepticism towards Santa Rosalia, or why are there so few kinds of animals? Evolution 35: 124–138.

    Google Scholar 

  • Hamilton, W.D. & M. Zuk, 1982. Heritable true fitness and bright birds: a role for parasites. Science 218: 384–387.

    Google Scholar 

  • Harrison, R.G., 1993. Hybrid Zones and the Evolutionary Process. Oxford University Press, New York.

    Google Scholar 

  • Hawthorne, D.J. & S. Via, 2001. Genetic linkage of ecological specialization and reproductive isolation in pea aphids. Nature 412: 904–907.

    Google Scholar 

  • Higa, I. & Y. Fuyama, 1993. Genetics of food preference in Drosophila sechellia. I. Responses to food attractants. Genetica 88: 129–136.

    Google Scholar 

  • Hostert, E.E., 1997. Reinforcement: a new perspective on an old controversy. Evolution 51: 697–702.

    Google Scholar 

  • Hutter, C.M. & D.M. Rand, 1995. Competition between mitochondrial haplotypes in distinct nuclear genetic environments: Drosophila pseudoobscura v.s. D. persimilis. Genetics 140: 537–548.

    Google Scholar 

  • Johnson, N.A., 2000. Gene interactions and the origin of species, pp. 197–212 in Epistasis and the Evolutionary Process, edited by I.B. Wolf, E.D. Brodie & M. Wade. Oxford University Press, New York.

    Google Scholar 

  • Jones, C., 1998. The genetic basis of Drosophila sechellia's resistance to a host plant toxin. Genetics 149: 1899–1908.

    Google Scholar 

  • Kirkpatrick, M., 1982. Sexual selection and the evolution of female choice. Evolution 36: 1–12.

    Google Scholar 

  • Kirkpatrick, M. & N.H. Barton, 1997. The strength of indirect selection on female mating preferences. P. Natl. Acad. Sci. USA 94: 1282–1286.

    Google Scholar 

  • Kirkpatrick, M. & V. Ravigné, 2002. Speciation by natural and sexual selection. Am. Nat. 159: 522–535.

    Google Scholar 

  • Kliman, R.M., P. Andolfatto, J.A. Coyne, F. Depaulis, M. Kreitman, A.J. Berry, J. McCarter, J. Wakeley & J. Hey, 2000. The population genetics of the origin and divergence of the Drosophila simulans complex species. Genetics 156: 1913–1931.

    Google Scholar 

  • Kotiaho, J.S., L.W. Simmons & J.L. Tomkins, 2001. Towards a resolution of the lek paradox. Nature 410: 684–686.

    Google Scholar 

  • Lande, R., 1981. Models of speciation by sexual selection on polygenic traits. P. Natl. Acad. Sci. USA 78: 3721–3725.

    Google Scholar 

  • Li, W.H. & M. Nei, 1974. Stable linkage disequilibrium without epistasis in subdivided populations. Theor. Popul. Biol. 6: 173–183.

    Google Scholar 

  • Li, Z., S.R.M. Pinson, A.H. Paterson, W.D. Park & J.W. Stansel, 1997. Genetics of hybrid sterility and hybrid breakdown in an intersubspecific rice (Oryza sativa L.) population. Genetics 145: 1139–1148.

    Google Scholar 

  • Lindsley, D.L. & L. Sandler, 1977. The genetic analysis of meiosis in female Drosophila melanogaster. Philos. T. Roy. Soc. B 277: 295–312.

    Google Scholar 

  • Liou, L.W. & T.D. Price, 1994. Speciation by reinforcement of premating isolation. Evolution 48: 1451–1459.

    Google Scholar 

  • Machado, C.A., R.M. Kliman, J.A. Markert & J. Hey, 2002. Inferring the history of speciation from multilocus sequence data: the case of Drosophila pseudoobscura and its close relatives. Mol. Biol. Evol. 19: 472–488.

    Google Scholar 

  • Mallet, J., 1995. A species definition for the modern synthesis. Trends Ecol. Evol. 10: 294–299.

    Google Scholar 

  • Mayr, E., 1963. Animal Species and Evolution. Belknap Press, Cambridge, MA.

    Google Scholar 

  • Nachman, M.W. & G.A. Churchill, 1996. Heterogeneity in rates of recombination across the mouse genome. Genetics 142: 537–548.

    Google Scholar 

  • Nitao, J.K., M.P. Ayres, R.C. Laderhouse & J.M. Scriber, 1991. Larval adaptation to lauraceosus hosts: geographic divergence in the spicebush swallowtail butterfly. Ecology 72: 1428–1435.

    Google Scholar 

  • Noor, M.A.F., 1997. Genetics of sexual isolation and courtship dysfunction in male hybrids of Drosophila pseudoobscura and D. persimilis. Evolution 51: 809–815.

    Google Scholar 

  • Noor, M.A.F., A.L. Cunningham & J.C. Larkin, 2001a. Consequences of recombination rate variation on quantitative trait locus mapping studies: simulations based on the Drosophila melanogaster genome. Genetics 159: 581–588.

    Google Scholar 

  • Noor, M.A.F., K.L. Grams, L.A. Bertucci, Y. Almendarez, J. Reiland & K.R. Smith, 2001b. The genetics of reproductive isolation and the potential for gene exchange between Drosophila pseudoobscura and D. persimilis via backcross hybrid males. Evolution 55: 512–521.

    Google Scholar 

  • Noor, M.A.F., K.L. Grams, L.A. Bertucci & J. Reiland, 2001c. Chromosomal inversions and the reproductive isolation of species. P. Natl. Acad. Sci. USA 98: 12084–12088.

    Google Scholar 

  • Otto, S.P., 1991. On evolution under sexual and viability selection: a two-locus diploid model. Evolution 45: 1443–1457.

    Google Scholar 

  • Palopoli, M.F. & C.-I. Wu, 1994. Genetics of hybrid male sterility between Drosophila sibling species: a complex web of epistasis is revealed in interspecific studies. Genetics 138: 329–341.

    Google Scholar 

  • Palopoli, M.F., A.W. Davis & C.-I. Wu, 1996. Discord between the phylogenies inferred from molecular versus functional data: uneven rates of functional evolution or low levels of gene flow? Genetics 144: 1321–1328.

    Google Scholar 

  • Payseur, B.A. & M.W. Nachman, 2000. Microsatellite variation and recombination rate in the human genome. Genetics 156: 1285–1298.

    Google Scholar 

  • Perez, D.E., C.-I. Wu, N.A. Johnson & M.-L. Wu, 1993. Genetics of reproductive isolation in the Drosophila simulans clade: DNA marker-assisted mapping and characterization of a hybrid-male sterility gene, Odysseus (Ods). Genetics 134: 261–275.

    Google Scholar 

  • Powell, J.R., 1983. Interspecific cytoplasmic gene flow in the absence of nuclear gene flow: evidence from Drosophila. P. Natl. Acad. Sci. USA 80: 492–495.

    Google Scholar 

  • Pritchard, J.K. & M. Przeworski, 2001. Linkage disequilibrium in humans: models and data. Am. J. Hum Genet. 69: 1–14.

    Google Scholar 

  • Rice, W.R. & E.E. Hostert, 1993. Laboratory experiments on speciation: what have we learned in forty years? Evolution 47: 1637–1653.

    Google Scholar 

  • Rieseberg, L.H., 2001. Chromosomal rearrangements and speciation. Trends Ecol. Evol. 16: 351–358.

    Google Scholar 

  • Rieseberg, L.H., J. Whitton & K. Gardner, 1999. Hybrid zones and the genetic architecture of a barrier to gene flow between two sunflower species. Genetics 152: 713–727.

    Google Scholar 

  • Roulin, A., T.W. Jungi, H. Pfister & E. Dijkstra, 2000. Female barn owls (Tyto alba) advertise good genes. P. Roy. Soc. Lond. B 267: 937–941.

    Google Scholar 

  • Sanderson, N., 1989. Can gene flow prevent reinforcement? Evolution 43: 1223–1235.

    Google Scholar 

  • Schaeffer, S.W. & E.L. Miller, 1991. Nucleotide sequence analysis of Adh genes estimates the time of geographic isolation of the Bogota population of Drosophila pseudoobscura. P. Natl. Acad. Sci. USA 88: 6097–6101.

    Google Scholar 

  • Scriber, J.M., 1986. Allelochemicals and alimentary ecology: heterosis in a hybrid zone? in Molecular Aspects of Insect-Plant Associations, edited by L.B. Brattsten & S. Admad. Plenum, New York.

    Google Scholar 

  • Scriber, J.M., B.L. Giebink & D. Snider, 1991. Reciprocal latitudinal clines in ovisposition behavior of Papilo glaucus and P. canadensis across the Great Lakes hybrid zone: possible sex-linkage of oviposition preferences. Oecologia 81: 360–368.

    Google Scholar 

  • Servedio, M.R., 2000. Reinforcement and the genetics of nonrandom mating. Evolution 54: 21–29.

    Google Scholar 

  • Sezer, M. & R.K. Butlin, 1998. The genetic basis of oviposition preference differences between sympatric host races of the brown planthopper (Nilaparvata lugens). P. Roy. Soc. Lond. B 265: 2399–2405.

    Google Scholar 

  • Shaw, D.D., P. Wilkinson & C. Moran, 1983. A comparison of chromosomal and allozymal variation across a narrow hybrid zone in the grasshopper Caledia captiva. Chromosoma 75: 333–351.

    Google Scholar 

  • Singer, M.C., D. Ng & C.D. Thomas, 1988. Heritability of oviposition preference and its relationship to offspring performance within a single insect population. Evolution 42: 977–985.

    Google Scholar 

  • Takimoto, G., M. Higashi & N. Yamamura, 2000. A deterministic genetic model for sympatric speciation by sexual selection. Evolution 54: 1870–1881.

    Google Scholar 

  • Taylor, C.E. & J.R. Powell, 1978. Habitat choice in natural populations of Drosophila. Oecologia 37: 69–75.

    Google Scholar 

  • Thompson, J.N., ed, 1994. The Coevolutionary Process. The University of Chicago Press, Chicago.

    Google Scholar 

  • Thompson, J.N., W. Wehling & R. Podolsky, 1990. Evolutionary genetics of host use in swallowtail butterflies. Nature 148–150.

  • Ting, C.-T., S.-C. Tsaur & C.-I. Wu, 2000. The phylogeny of closely related species as revealed by the genealogy of a speciation gene, Odysseus. P. Natl. Acad. Sci. USA 97: 5313–5316.

    Google Scholar 

  • Trickett, A.J. & R.K. Butlin, 1994. Recombination suppressors and the evolution of new species. Heredity 73: 339–345.

    Google Scholar 

  • Turner, J.R.G., 1967. The evolution of supergenes. Am. Nat.: 195–228.

  • Turner, J.R.G., 1967. Why does the genotype not congeal? Evolution 21: 645–656.

    Google Scholar 

  • Via, S., 1990. Ecological genetics and host adaptation in herbivorous insects-the experimental-study of evolution in natural and agricultural systems. Annu. Rev. Entomol. 35: 421–446.

    Google Scholar 

  • Wallace, B.M.N. & J.B. Searle, 1994. Oogenesis in homozygotes and heterozygotes for robertsonian chromosomal rearrangements from natural-populations of the common shrew, Sorex-araneus. J. Reprod. Fertil. 100: 231–237.

    Google Scholar 

  • Wang, R.L., J. Wakeley & J. Hey, 1997. Gene flow and natural selection in the origin of Drosophila pseudoobscura and close relatives. Genetics 147: 1091–1106.

    Google Scholar 

  • Welch, A.M., R.D. Semlitsch & H.C. Gerhardt, 1998. Call duration as an indicator of genetic quality in male gray tree frogs. Science 280: 1928–1930.

    Google Scholar 

  • Wu, C.-I. & H. Hollocher, 1998. Subtle is nature: the genetics of species differentiation and speciation, pp. 339–351 in Endless Forms: Species and Speciation, edited by D.J. Howard & S.H. Berlocher. Oxford University Press, New York.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Louisiana State University, 107 Life Sciences Building, Baton Rouge, LA, 70803, USA (Phone

    Daniel Ortíz-Barrientos, Jane Reiland & Mohamed A.F. Noor

  2. Department of Genetics, Rutgers University, Piscataway, NJ, 08854, USA

    Jody Hey

Authors
  1. Daniel Ortíz-Barrientos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jane Reiland
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jody Hey
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mohamed A.F. Noor
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ortíz-Barrientos, D., Reiland, J., Hey, J. et al. Recombination and the Divergence of Hybridizing Species. Genetica 116, 167–178 (2002). https://doi.org/10.1023/A:1021296829109

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1021296829109

Search

Navigation