Skip to main content
Genetics logoLink to Genetics
. 1999 May;152(1):355–371. doi: 10.1093/genetics/152.1.355

Introgression through rare hybridization: A genetic study of a hybrid zone between red and sika deer (genus Cervus) in Argyll, Scotland.

S J Goodman 1, N H Barton 1, G Swanson 1, K Abernethy 1, J M Pemberton 1
PMCID: PMC1460577  PMID: 10224266

Abstract

In this article we describe the structure of a hybrid zone in Argyll, Scotland, between native red deer (Cervus elaphus) and introduced Japanese sika deer (Cervus nippon), on the basis of a genetic analysis using 11 microsatellite markers and mitochondrial DNA. In contrast to the findings of a previous study of the same population, we conclude that the deer fall into two distinct genetic classes, corresponding to either a sika-like or red-like phenotype. Introgression is rare at any one locus, but where the taxa overlap up to 40% of deer carry apparently introgressed alleles. While most putative hybrids are heterozygous at only one locus, there are rare multiple heterozygotes, reflecting significant linkage disequilibrium within both sika- and red-like populations. The rate of backcrossing into the sika population is estimated as H = 0.002 per generation and into red, H = 0.001 per generation. On the basis of historical evidence that red deer entered Kintyre only recently, a diffusion model evaluated by maximum likelihood shows that sika have increased at approximately 9.2% yr-1 from low frequency and disperse at a rate of approximately 3.7 km yr-1. Introgression into the red-like population is greater in the south, while introgression into sika varies little along the transect. For both sika- and red-like populations, the degree of introgression is 30-40% of that predicted from the rates of current hybridization inferred from linkage disequilibria; however, in neither case is this statistically significant evidence for selection against introgression.

Full Text

The Full Text of this article is available as a PDF (335.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abernethy K. The establishment of a hybrid zone between red and sika deer (genus Cervus). Mol Ecol. 1994 Dec;3(6):551–562. doi: 10.1111/j.1365-294x.1994.tb00086.x. [DOI] [PubMed] [Google Scholar]
  2. Asmussen M. A., Arnold J. The effects of admixture and population subdivision on cytonuclear disequilibria. Theor Popul Biol. 1991 Jun;39(3):273–300. doi: 10.1016/0040-5809(91)90024-a. [DOI] [PubMed] [Google Scholar]
  3. Barbujani G., Pilastro A., De Domenico S., Renfrew C. Genetic variation in North Africa and Eurasia: neolithic demic diffusion vs. Paleolithic colonisation. Am J Phys Anthropol. 1994 Oct;95(2):137–154. doi: 10.1002/ajpa.1330950203. [DOI] [PubMed] [Google Scholar]
  4. Barton N. H., Hewitt G. M. Adaptation, speciation and hybrid zones. Nature. 1989 Oct 12;341(6242):497–503. doi: 10.1038/341497a0. [DOI] [PubMed] [Google Scholar]
  5. Barton N., Bengtsson B. O. The barrier to genetic exchange between hybridising populations. Heredity (Edinb) 1986 Dec;57(Pt 3):357–376. doi: 10.1038/hdy.1986.135. [DOI] [PubMed] [Google Scholar]
  6. Bishop M. D., Kappes S. M., Keele J. W., Stone R. T., Sunden S. L., Hawkins G. A., Toldo S. S., Fries R., Grosz M. D., Yoo J. A genetic linkage map for cattle. Genetics. 1994 Feb;136(2):619–639. doi: 10.1093/genetics/136.2.619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brookfield J. F. A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol. 1996 Jun;5(3):453–455. doi: 10.1111/j.1365-294x.1996.tb00336.x. [DOI] [PubMed] [Google Scholar]
  8. Buchanan F. C., Crawford A. M. Ovine microsatellites at the OarFCB11, OarFCB128, OarFCB193, OarFCB266 and OarFCB304 loci. Anim Genet. 1993 Apr;24(2):145–145. doi: 10.1111/j.1365-2052.1993.tb00269.x. [DOI] [PubMed] [Google Scholar]
  9. Chakraborty R., De Andrade M., Daiger S. P., Budowle B. Apparent heterozygote deficiencies observed in DNA typing data and their implications in forensic applications. Ann Hum Genet. 1992 Jan;56(Pt 1):45–57. doi: 10.1111/j.1469-1809.1992.tb01128.x. [DOI] [PubMed] [Google Scholar]
  10. Crawford A. M., Dodds K. G., Ede A. J., Pierson C. A., Montgomery G. W., Garmonsway H. G., Beattie A. E., Davies K., Maddox J. F., Kappes S. W. An autosomal genetic linkage map of the sheep genome. Genetics. 1995 Jun;140(2):703–724. doi: 10.1093/genetics/140.2.703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Emerson B. C., Tate M. L. Genetic analysis of evolutionary relationships among deer (subfamily Cervinae). J Hered. 1993 Jul-Aug;84(4):266–273. doi: 10.1093/oxfordjournals.jhered.a111338. [DOI] [PubMed] [Google Scholar]
  12. Gaszner P., Past T., Juhász P., Jávor T. Gyógyszerkinetikai vizsgálatok nagydosisú (70-920 mg) atropin adása során, 3H atropin izotóp méréssel (1. A máj depó-szerepe) Orv Hetil. 1976 Aug 15;117(33):1988–1991. [PubMed] [Google Scholar]
  13. Grosse W. M., Finlay O., Kossarek L. M., Clark T. G., McGraw R. A. Five bovine microsatellite markers derived from skeletal muscle cDNA: RME01, RME11, RME23, RME25 and RME33. Anim Genet. 1995 Apr;26(2):126–127. doi: 10.1111/j.1365-2052.1995.tb02652.x. [DOI] [PubMed] [Google Scholar]
  14. Gyllenstein U., Ryman N., Reuterwall C., Dratch P. Genetic differentiation in four European subspecies of red deer (Cervus elaphus L.). Heredity (Edinb) 1983 Dec;51(Pt 3):561–580. doi: 10.1038/hdy.1983.71. [DOI] [PubMed] [Google Scholar]
  15. Kaplan N. L., Hill W. G., Weir B. S. Likelihood methods for locating disease genes in nonequilibrium populations. Am J Hum Genet. 1995 Jan;56(1):18–32. [PMC free article] [PubMed] [Google Scholar]
  16. Kocher T. D., Thomas W. K., Meyer A., Edwards S. V., Päbo S., Villablanca F. X., Wilson A. C. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci U S A. 1989 Aug;86(16):6196–6200. doi: 10.1073/pnas.86.16.6196. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Linnell J. C., Cross T. F. The biochemical systematics of red and sika deer (genus Cervus) in Ireland. Hereditas. 1991;115(3):267–273. doi: 10.1111/j.1601-5223.1992.tb00569.x. [DOI] [PubMed] [Google Scholar]
  18. Mommens G., Coppieters W., Van de Weghe A., Van Zeveren A., Bouquet Y. Dinucleotide repeat polymorphism at the bovine MM12E6 and MM8D3 loci. Anim Genet. 1994 Oct;25(5):368–368. doi: 10.1111/j.1365-2052.1994.tb00381.x. [DOI] [PubMed] [Google Scholar]
  19. Moore S. S., Sargeant L. L., King T. J., Mattick J. S., Georges M., Hetzel D. J. The conservation of dinucleotide microsatellites among mammalian genomes allows the use of heterologous PCR primer pairs in closely related species. Genomics. 1991 Jul;10(3):654–660. doi: 10.1016/0888-7543(91)90448-n. [DOI] [PubMed] [Google Scholar]
  20. Nagata J., Masuda R., Kaji K., Kaneko M., Yoshida M. C. Genetic variation and population structure of the Japanese sika deer (Cervus nippon) in Hokkaido Island, based on mitochondrial D-loop sequences. Mol Ecol. 1998 Jul;7(7):871–877. doi: 10.1046/j.1365-294x.1998.00404.x. [DOI] [PubMed] [Google Scholar]
  21. Nagylaki T. Conditions for the existence of clines. Genetics. 1975 Jul;(3):595–615. doi: 10.1093/genetics/80.3.595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Paterson S., Pemberton J. M. No evidence for major histocompatibility complex-dependent mating patterns in a free-living ruminant population. Proc Biol Sci. 1997 Dec 22;264(1389):1813–1819. doi: 10.1098/rspb.1997.0250. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Pemberton J. M., Slate J., Bancroft D. R., Barrett J. A. Nonamplifying alleles at microsatellite loci: a caution for parentage and population studies. Mol Ecol. 1995 Apr;4(2):249–252. doi: 10.1111/j.1365-294x.1995.tb00214.x. [DOI] [PubMed] [Google Scholar]
  24. Pierson C. A., Ede A. J., Crawford A. M. Ovine microsatellites at the OarHH30, OarHH51, OarVH54, OarCP88, OarCP93, OarCP134 loci. Anim Genet. 1994 Aug;25(4):294–295. doi: 10.1111/j.1365-2052.1994.tb00224.x. [DOI] [PubMed] [Google Scholar]
  25. Slate J., Coltman D. W., Goodman S. J., MacLean I., Pemberton J. M., Williams J. L. Bovine microsatellite loci are highly conserved in red deer (Cervus elaphus), sika deer (Cervus nippon) and Soay sheep (Ovis aries). Anim Genet. 1998 Aug;29(4):307–315. doi: 10.1046/j.1365-2052.1998.00347.x. [DOI] [PubMed] [Google Scholar]
  26. Tate M. L., Mathias H. C., Fennessy P. F., Dodds K. G., Penty J. M., Hill D. F. A new gene mapping resource: interspecies hybrids between Père David's deer (Elaphurus davidianus) and red deer (Cervus elaphus). Genetics. 1995 Mar;139(3):1383–1391. doi: 10.1093/genetics/139.3.1383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Turelli M., Barton N. H. Genetic and statistical analyses of strong selection on polygenic traits: what, me normal? Genetics. 1994 Nov;138(3):913–941. doi: 10.1093/genetics/138.3.913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Yasuda N., Kimura M. A gene-counting method of maximum likelihood for estimating gene frequencies in ABO and ABO-like systems. Ann Hum Genet. 1968 May;31(4):409–420. doi: 10.1111/j.1469-1809.1968.tb00574.x. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES