Hybrid Zones

Takeshi Kawakami, Uppsala University, Uppsala, Sweden
Roger K Butlin, University of Sheffield, Sheffield, UK

Published online: January 2012

DOI: 10.1002/9780470015902.a0001752.pub2

A hybrid zone occurs where two distinct genetic forms meet, mate and produce offspring with mixed genomes. Such zones may vary in width, length and patchiness, and are found between species, subspecies, races or forms. Stable hybrid zones may be maintained by selection against hybrids, environmental selection, or a combination of the two. A hybrid zone can arise either by direct environmental selection in contiguous populations or by renewed contact between previously isolated populations. Hybrid zones act as semi‐permeable barriers, which allow gene exchange for neutral or adaptive characters, whereas restricting introgression of alleles that contribute to local adaptation or reduced hybrid fitness. The study of genomic regions that experience barriers to gene flow can provide an important window for identifying specific genes and mutations that underlie reproductive isolation and local adaptation. With the help of recent technological advances in development of thousands of molecular markers, distributed genome‐wide, identification of such genomic regions is becoming possible in natural hybrid zones.

Key Concepts:

  • A hybrid zone is a narrow geographic region where two genetically distinct populations or species are found in close proximity and hybridise to produce offspring of mixed ancestry.
  • Hybrid zones are widespread, both geographically and across animal and plant taxa.
  • A hybrid zone is maintained by a balance between selection and dispersal.
  • Selective forces can be intrinsic (e.g. selection against less‐fit hybrids) or extrinsic (e.g. environment‐dependent selection).
  • Spatial analysis of allele‐frequency clines across a hybrid zone provides estimates of important population genetic parameters (e.g. selection, dispersal and linkage disequilibrium).
  • Surveys of differential gene flow across a hybrid zone have the potential to localise genomic regions that habour genes responsible for barriers to gene exchange.

Keywords: hybrid zones; divergence; speciation; selection; dispersal; population density; phylogeography

Figure 1. The hybrid zone in M. m. musculus and M. m. domesticus. (a) The solid purple line indicates the location of the hybrid zone. An approximate position of the Norwegian/Swedish zone is shown as a dashed line. Six extensively studied transects are shown as yellow rectangles. (b) The detailed location of the hybrid zone at the Czech transect (D). Red circles indicate 228 sampling sites. The yellow dashed line depicts the course of the zone based on consensus of six autosomal and nine X‐linked loci. Map by courtesy of Miloš Macholán.
Figure 2. Effects of environment on hybrid zone structure and position. Two genotypes strongly adapted to two distinct habitats with sample transects taken across (a) a linear zone and (b) a mosaic zone. (c, d) The respective character clines resulting from these transects. Note differences in width and shape. (e) The distribution of individuals through a low‐density region, where the zone is not at the density trough and (f) the dispersal of parental types (arrows) to bring the hybrid zone to rest in the centre of the density trough.
Figure 3. Shape of sigmoid and stepped clines (blue and red lines, respectively). Widths of each cline (w1 and w2) are measured as the inverse of the maximum slope (dashed lines) at the centre of the zone (c) (i.e. w1>w2). A sigmoid cline consists only of a hyperbolic tangent function (tanh), whereas a stepped cline consists of a steep central region, defined by a tanh function, and shallow tails of introgression, defined by an exponential function. Note that the extent of introgression at the left and right tails can be similar to (symmetric stepped cline) or different from each other (asymmetric stepped cline).
Figure 4. Phylogeography of European hedgehogs. (a) The ranges of Erinaceus europeus (west) and Erinaceus concolor (east), with (b) an mtDNA‐cytb phylogeny superimposed. Note the deep divergence (12%) between the nominate species, and their cryptic subdivision into further distinct (6%) clades. This indicates separate survival in Mediterranean refugia over several ice ages.
close
 References
    Alexandrino J, Baird SJE, Lawson L et al. (2005) Strong selection against hybrids at a hybrid zone in the Ensatina ring species complex and its evolutionary implications. Evolution 59: 1334–1347.
    book Baird SJE and Macholán M (2012) "What can the Mus musculus musculus/M. m. domesticus hybrid zone tell us about speciation"? In: Macholán M, Baird SJE, Munclinger P and Piálek J (eds) Evolution of the House Mouse. Cambridge Studies in Morphology and Molecules: New Paradigms in Evolutionary Biology. Cambridge: Cambridge University Press (in press).
    book Barton NH and Gale KS (1993) "Genetic analysis of hybrid zones". In: Harrison RG (ed.) Hybrid Zones and the Evolutionary Process, pp. 13–45. New York: Oxford University Press.
    Barton NH and Hewitt GM (1981) A chromosomal cline in the grasshopper Podisma pedestris. Evolution 35: 1008–1018.
    Barton NH and Hewitt GM (1985) Analysis of hybrid zones. Annual Review of Ecology and Systematics 16: 113–148.
    Bímová BV, Macholán M, Baird SJE et al. (2011) Reinforcement selection acting on the European house mouse hybrid zone. Molecular Ecology 20: 2403–2424.
    Blum MJ (2002) Rapid movement of a Heliconius hybrid zone: evidence for phase III of Wright's shifting balance theory? Evolution 56: 1992–1998.
    Bozikova E, Munclinger P, Teeter KC et al. (2005) Mitochondrial DNA in the hybrid zone between Mus musculus musculus and Mus musculus domesticus: a comparison of two transects. Biological Journal of the Linnean Society 84: 363–378.
    Britton‐Davidian J, Catalan J, Ramalhinho MD et al. (2005) Chromosomal phylogeny of Robertsonian races of the house mouse on the island of Madeira: testing between alternative mutational processes. Genetical Research 86: 171–183.
    book Butlin RK (1998) "What do hybrid zones in general, and the Chorthippus parallelus zone in particular, tell us about speciation"? In: Howard DJ and Berlocher SH (eds) Endless Forms: Species and Speciation, pp. 367–377. New York: Oxford University Press.
    Cruzan MB and Arnold ML (1993) Ecological and genetic associations in an Iris hybrid zone. Evolution 47: 1432–1445.
    Cucchi T, Vigne JD and Auffray JC (2005) First occurrence of the house mouse (Mus musculus domesticus Schwarz & Schwarz, 1943) in the Western Mediterranean: a zooarchaeological revision of subfossil occurrences. Biological Journal of the Linnean Society 84: 429–445.
    Durrett R, Buttel L and Harrison R (2000) Spatial models for hybrid zones. Heredity 84: 9–19.
    other Duvaux L, Belkhir K, Boulesteix M et al. (in press) Isolation and gene flow: inferring the speciation history of European house mice. Molecular Ecology. doi: 10.1111/j.1365‐294X.2011.05343.x
    Elias M, Joron M, Willmott K et al. (2009) Out of the Andes: patterns of diversification in clearwing butterflies. Molecular Ecology 18: 1716–1729.
    Ferris SD, Sage RD, Huang CM et al. (1983) Flow of mitochondrial DNA across a species boundary. Proceedings of the National Academy of Sciences of the USA 80: 2290–2294.
    Geraldes A, Basset P, Gibson B et al. (2008) Inferring the history of speciation in house mice from autosomal, X‐linked, Y‐linked and mitochondrial genes. Molecular Ecology 17: 5349–5363.
    Gompert Z and Buerkle CA (2010) INTROGRESS: a software package for mapping components of isolation in hybrids. Molecular Ecology Resources 10: 378–384.
    book Harrison RG (1993) Hybrid Zones and the Evolutionary Process. Oxford: Oxford University Press.
    Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society of London Series B – Biological Sciences 359: 183–195.
    Hofman S and Szymura JM (2007) Limited mitochondrial DNA introgression in a Bombina hybrid zone. Biological Journal of the Linnean Society 91: 295–306.
    Jiggins CD and Mallet J (2000) Bimodal hybrid zones and speciation. Trends in Ecology & Evolution 15: 250–255.
    Johannesson K, Panova M, Kemppainen P et al. (2010) Repeated evolution of reproductive isolation in a marine snail: unveiling mechanisms of speciation. Philosophical Transactions of the Royal Society B – Biological Sciences 365: 1735–1747.
    Kawakami T, Butlin RK, Adams M et al. (2009) Genetic analysis of a chromosomal hybrid zone in the Australian morabine grasshoppers (Vandiemenella, viatica species group). Evolution 63: 139–152.
    Keller I, Veltsos P and Nichols RA (2008) The frequency of rDNA variants within individuals provides evidence of population history and gene flow across a grasshopper hybrid zone. Evolution 62: 833–844.
    Macholán M, Baird SJE, Dufková P et al. (2011) Assessing multilocus introgression patterns: a case study on the mouse X chromosome in central Europe. Evolution 65: 1428–1446.
    Macholán M, Baird SJE, Munclinger P et al. (2008) Genetic conflict outweighs heterogametic incompatibility in the mouse hybrid zone? BMC Evolutionary Biology 8: 271.
    Macholán M, Munclinger P, Sugerkova M et al. (2007) Genetic analysis of autosomal and X‐linked markers across a mouse hybrid zone. Evolution 61: 746–771.
    Maroja LS, Andres JA and Harrison RG (2009) Genealogical discordance and patterns of introgression and selection across a cricket hybrid zone. Evolution 63: 2999–3015.
    Moritz C, Hoskin CJ, MacKenzie JB et al. (2009) Identification and dynamics of a cryptic suture zone in tropical rainforest. Proceedings of the Royal Society B – Biological Sciences 276: 1235–1244.
    Moulia C, Aussel JP, Bonhomme F et al. (1991) Wormy mice in a hybrid zone – a genetic control of susceptibility to parasite infection. Journal of Evolutionary Biology 4: 679–687.
    Pavlova SV (2010) A distinct chromosome race of the common shrew (Sorex araneus Linnaeus, 1758) within the Arctic Circle in European Russia. Comparative Cytogenetics 4: 73–78.
    Payseur BA and Nachman MW (2005) The genomics of speciation: investigating the molecular correlates of X chromosome introgression across the hybrid zone between Mus domesticus and Mus musculus. Biological Journal of the Linnean Society 84: 523–534.
    Piálek J, Hauffe HC and Searle JB (2005) Chromosomal variation in the house mouse. Biological Journal of the Linnean Society 84: 535–563.
    Rand DM and Harrison RG (1989) Ecological genetics of a mosaic hybrid zone: mitochondrial, nuclear, and reproductive differentiation of crickets by soil type. Evolution 43: 432–449.
    Raufaste N, Orth A, Belkhir K et al. (2005) Inferences of selection and migration in the Danish house mouse hybrid zone. Biological Journal of the Linnean Society 84: 593–616.
    Rieseberg LH, Whitton J and Gardner K (1999) Hybrid zones and the genetic architecture of a barrier to gene flow between two sunflower species. Genetics 152: 713–727.
    Riginos C and Cunningham CW (2005) Local adaptation and species segregation in two mussel (Mytilus edulis×Mytilus trossulus) hybrid zones. Molecular Ecology 14: 381–400.
    Saetre GP and Saether SA (2010) Ecology and genetics of speciation in Ficedula flycatchers. Molecular Ecology 19: 1091–1106.
    Sage RD, Heyneman D, Lim KC et al. (1986) Wormy mice in a hybrid zone. Nature 324: 60–63.
    Seddon JM, Santucci F, Reeve NJ et al. (2001) DNA footprints of European hedgehogs, Erinaceus europaeus and E. concolor: Pleistocene refugia, postglacial expansion and colonization routes. Molecular Ecology 10: 2187–2198.
    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.
    Shuker DM, Underwood K, King TM et al. (2005) Patterns of male sterility in a grasshopper hybrid zone imply accumulation of hybrid incompatibilities without selection. Proceedings of the Royal Society B – Biological Sciences 272: 2491–2497.
    Sites JW, Barton NH and Reed KM (1995) The genetic structure of a hybrid zone between two chromosome races of the Sceloporus grammicus complex (Sauria, Phrynosomatidae) in central Mexico. Evolution 49: 9–36.
    Smadja C and Ganem G (2005) Asymmetrical reproductive character displacement in the house mouse. Journal of Evolutionary Biology 18: 1485–1493.
    Smadja C and Ganem G (2008) Divergence of odorant signals within and between the two European subspecies of the house mouse. Behavioral Ecology 19: 223–230.
    book Szymura JM (1993) "Analysis of hybrid zones with Bombina". In: Harrison RG (ed.) Hybrid Zones and the Evolutionary Process, pp. 261–289. New York: Oxford University Press.
    Teeter KC, Thibodeau LM, Gompert Z et al. (2010) The variable genomic architecture of isolation between hybridizing species of house mice. Evolution 64: 472–485.
    Vyskočilová M, Pražanová G and Piálek J (2009) Polymorphism in hybrid male sterility in wild‐derived Mus musculus musculus strains on proximal chromosome 17. Mammalian Genome 20: 83–91.
    Yanchukov A, Hofman S, Szymura JM et al. (2006) Hybridization of Bombina bombina and B. variegata (Anura, Discoglossidae) at a sharp ecotone in western Ukraine: comparisons across transects and over time. Evolution 60: 583–600.
 Further Reading
    book Arnold ML (2006) Evolution Through Genetic Exchange. Oxford: Oxford University Press.
    Buggs RJA (2007) Empirical study of hybrid zone movement. Heredity 99: 301–312.
    book Coyne JA and Orr HA (2004) Speciation. Sunderland, MA: Sinauer Associates.
    book Endler JA (1977) Geographic Variation, Speciation, and Clines. Princeton, NJ: Princeton University Press.
    Harrison RG (1990) Hybrid zones: windows on evolutionary processes. Oxford Surveys in Evolutionary Biology 7: 69–128.
    Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405: 907–913.
    book Macholán M, Baird SJE, Munclinger P and Piálek J (eds) (2012) Evolution of the House Mouse. Cambridge Studies in Morphology and Molecules: New Paradigms in Evolutionary Biology. Cambridge: Cambridge University Press.
    Noor MAF and Feder JL (2006) Speciation genetics: evolving approaches. Nature Reviews Genetics 7: 851–861.

Related Sub-Topics:

Evolution: Theories and Ideas | Selection and Variation | Population Structure and Genetics | Evolution of Species | Evolutionary Ecology
Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Hybrid Zones
 
How to Cite close
Kawakami, Takeshi, and Butlin, Roger K(Jan 2012) Hybrid Zones. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001752.pub2]