Reinforcement

Abstract

Reinforcement is the process, in which traits that increase pre‐zygotic isolation between two differentiated populations are favoured due to natural selection against the production of unfit hybrids or otherwise maladaptive interbreeding. It is a central process in many models of speciation and it is the only known process in which natural selection acts directly to promote speciation. Reinforcement was for long considered a controversial idea despite the fact that early theoretical models showed that the process could work under apparently realistic biological assumptions. Clarification of concepts along with the publications of refined theoretical models as well as convincing comparative and empirical case studies has more or less resolved the controversy; reinforcement works, but it is still debated how important it is in speciation.

Key Concepts:

  • Reinforcement is an increase in pre‐zygotic isolation between differentiated taxa caused by natural selection against maladaptive hybridisation.

  • Reinforcement may contribute to speciation in previously geographically isolated taxa that experience secondary contact as well as to parapatric and sympatric modes of speciation.

  • Reinforcement can lead to a sympatric divergence (character displacement) in any trait that reduces the likelihood of mating or fertilisation between diverging taxa, including secondary sexual traits, mating behaviour and traits affecting enzymatic communication between egg and sperm.

  • Population genetic models show that assortative mating can increase as a response to genetic incompatibilities at other loci, but the process is sensitive to recombination.

  • Factors that reduce recombination, including strong assortative mating, strong incompatibility selection and physical linkage promotes speciation by reinforcement.

  • Comparative evidence suggests that pre‐zygotic isolation is stronger in sympatric species pairs than in allopatric ones, consistent with reinforcement.

  • In well‐documented empirical cases of reinforcement genetic factors that reduce recombination has been identified and incompatibility selection tends to be strong.

Keywords: speciation; reproductive isolation; mate recognition; character displacement; assortative mating

Figure 1.

Conditions for reinforcement based on 30 runs of the Liou and Price simulation. Initial divergence in the male mating trait (measured in phenotypic standard deviations) was paralleled by divergence in female preference. There was free recombination. The possible outcomes were speciation by reinforcement, extinction of one of the starting populations, or merging of the populations due to hybridisation. From Liou and Price . Copyright © 1994 The Society for the Study of Evolution.

Figure 2.

The classic example of increased mating signal divergence between sympatric populations, in frogs of the genus Litoria in Australia. Litoria ewingi occurs in the west and L. verreauxi in the east, with a substantial area of overlap. Oscillograms of L. ewingi (E) and L. verreauxi (V) calls show how a marked difference in pulse number and rate is maintained throughout the area of sympatry despite the similarity between the calls of allopatric populations. From Littlejohn . Copyright © 1965 The Society for the Study of Evolution.

Figure 3.

The relationship between pre‐zygotic isolation and genetic distance (Nei's D) in (a) allopatric and (b) sympatric pairs of Drosophila species showing the markedly greater isolation among sympatric pairs at genetic distances of less than .5. From Coyne and Orr . Copyright © 1989 The Society for the Study of Evolution.

Figure 4.

Plumage comparisons between European flycatcher species from allopatric and sympatric localities (Pied flycatcher, Ficedula hypolenca and collared flycatcher, Ficedula albicollis). The pattern of sympatric character divergence has been attributed to reinforcement selection on female mate preferences (Sætre et al., ).

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References

Bakker TCM and Pomiankowski A (1995) The genetic basis of female mate preferences. Journal of Evolutionary Biology 8: 129–172.

Butlin RK (1989) Reinforcement of premating isolation. In: Otte D and Endler JA (eds) Speciation and Its Consequences, pp. 158–179. Sunderland, MA: Sinauer.

Cain ML, Andreasen V and Howard DJ (1999) Reinforcing selection is effective under a relatively broad set of conditions in a mosaic hybrid zone. Evolution 53: 1343–1353.

Coyne JA and Orr HA (1997) Patterns of speciation in Drosophila revisited. Evolution 51: 295–303.

Dobzhansky Th (1970) Genetics of the Evolutionary Process. New York: Columbia University Press.

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

Gulick JT (1888) Divergent evolution through cumulative segregation. Journal of the Linnean Society of London, Zoology 20: 189–274.

Hopkins R and Rausher MD (2012) Pollinator‐mediated selection on flower color allele drives reinforcement. Science 335: 1090–1092.

Howard DJ (1993) Reinforcement: origin, dynamics and fate of an evolutionary hypothesis. In: Harrison RG (ed) Hybrid Zones and the Evolutionary Process, pp. 46–69. New York: Oxford University Press.

Jiggins CD, Naisbit RE, Coe RL and Mallet J (2001) Reproductive isolation caused by colour pattern mimicry. Nature 411: 302–305.

Kelly JK and Noor MA (1996) Speciation by reinforcement: a model derived from studies of Drosophila. Genetics 143: 1485–1497.

Liou LW and Price TD (1994) Speciation by reinforcement of premating isolation. Evolution 48: 1451–1459.

Littlejohn MJ (1965) Premating isolation in the Hyla ewingi complex (Anura: Hylidae). Evolution 19: 234–243.

Machado CA and Hey J (2003) The causes of phylogenetic conflict in a classic Drosophila species group. Proceedings of the Royal Society of London, Series B 270: 1193–1202.

Mallet J (2007) Hybrid speciation. Nature 446: 279–283.

Noor MA (1995) Speciation driven by natural selection in Drosophila. Nature 375: 674–675.

Nosil P, Crespi BJ and Sandoval CP (2003) Reproductive isolation driven by the combined effects of ecological adaptation and reinforcement. Proceedings of the Royal Society of London, Series B 270: 1911–1918.

Olofsson H, Frame AM and Servedio MR (2011) Can reinforcement occur with a learned trait? Evolution 65: 1992–2003.

Ortiz‐Barrientos D, Counterman BA and Noor MAF (2004) The genetics of speciation by reinforcement. PLoS Biology 2: e416.

Pfennig KS (2003) A test of alternative hypotheses for the evolution of reproductive isolation between spadefoot toads: support for the reinforcement hypothesis. Evolution 57: 2842–2851.

Rice WR and Hostert EE (1993) Laboratory experiments on speciation: what have we learned in forty years? Evolution 47: 1637–1653.

Sætre G‐P, Borge T, Lindroos K et al. (2003) Sex chromosome evolution and speciation in Ficedula flycatchers. Proceedings of the Royal Society of London, Series B 270: 53–59.

Sætre G‐P, Moum T, Bures S et al. (1997) A sexually selected character displacement in flycatchers reinforces premating isolation. Nature 387: 589–592.

Sæther SA, Sætre G‐P, Borge T et al. (2007) Sex chromosome‐linked species recognition and evolution of reproductive isolation in flycatchers. Science 318: 95–97.

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

Servedio MR and Noor MAF (2003) The role of reinforcement in speciation: theory and data. Annual Review of Ecology, Evolution and Systematics 34: 339–364.

Servedio MR, Sæther SA and Sætre G‐P (2009) Reinforcement and learning. Evolutionary Ecology 23: 109–123.

Servedio MR and Sætre G‐P (2003) Speciation as a positive feedback loop between postzygotic and prezygotic barriers to gene flow. Proceedings of the Royal Society of London, Series B 270: 1473–1479.

Templeton AR (1981) Mechanisms of speciation: a population genetic approach. Annual Review of Ecology and Systematics 12: 23–48.

Turelli M, Barton NH and Coyne JA (2001) Theory and speciation. Trends in Ecology and Evolution 16: 330–343.

Wallace AR (1889) Darwinism: An Exposition of the Theory of Natural Selection with Some of its Applications. New York: Macmillan.

Further Reading

Barton NH and Hewitt GM (1985) Analysis of hybrid zones. Annual Review of Ecology and Systematics 16: 113–148.

Coyne JA and Orr HA (2004) Speciation. Sunderland, MA: Sinauer Associates.

Dobzhansky Th (1940) Speciation as a stage in evolutionary divergence. American Naturalist 74: 312–321.

Kirkpatrick M and Ravigné V (2002) Speciation by natural and sexual selection: models and experiments. American Naturalist 159: S22–S35.

Noor MAF (1999) Reinforcement and other consequences of sympatry. Heredity 83: 503–508.

Ortiz‐Barrientos D, Grealy A and Nosil P (2009) The genetics and ecology of reinforcement – implications for the evolution of prezygotic isolation in sympatry and beyond. Annals of the New York Academy of Sciences 1168: 156–182.

Paterson HE (1982) Perspective on speciation by reinforcement. South African Journal of Science 78: 53–57.

Qvarnström A and Bailey RI (2009) Speciation through evolution of sex‐linked genes. Heredity 102: 4–15.

Sætre G‐P and Sæther SA (2010) Ecology and genetics of speciation in Ficedula flycatchers. Molecular Ecology 19: 1091–1106.

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How to Cite close
Sætre, Glenn‐Peter(Sep 2012) Reinforcement. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001754.pub3]