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Genetics. Dec 2001; 159(4): 1833–1844.
PMCID: PMC1461893

Recombination, balancing selection and phylogenies in MHC and self-incompatibility genes.

Abstract

Using a coalescent model of multiallelic balancing selection with recombination, the genealogical process as a function of recombinational distance from a site under selection is investigated. We find that the shape of the phylogenetic tree is independent of the distance to the site under selection. Only the timescale changes from the value predicted by Takahata's allelic genealogy at the site under selection, converging with increasing recombination to the timescale of the neutral coalescent. However, if nucleotide sequences are simulated over a recombining region containing a site under balancing selection, a phylogenetic tree constructed while ignoring such recombination is strongly affected. This is true even for small rates of recombination. Published studies of multiallelic balancing selection, i.e., the major histocompatibility complex (MHC) of vertebrates, gametophytic and sporophytic self-incompatibility of plants, and incompatibility of fungi, all observe allelic genealogies with unexpected shapes. We conclude that small absolute levels of recombination are compatible with these observed distortions of the shape of the allelic genealogy, suggesting a possible cause of these observations. Furthermore, we illustrate that the variance in the coalescent with recombination process makes it difficult to locate sites under selection and to estimate the selection coefficient from levels of variability.

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Selected References

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  • Dwyer KG, Balent MA, Nasrallah JB, Nasrallah ME. DNA sequences of self-incompatibility genes from Brassica campestris and B. oleracea: polymorphism predating speciation. Plant Mol Biol. 1991 Mar;16(3):481–486. [PubMed]
  • Emerson S. A Preliminary Survey of the Oenothera Organensis Population. Genetics. 1939 Jun;24(4):524–537. [PMC free article] [PubMed]
  • Griffiths RC, Marjoram P. Ancestral inference from samples of DNA sequences with recombination. J Comput Biol. 1996 Winter;3(4):479–502. [PubMed]
  • Hudson RR. Properties of a neutral allele model with intragenic recombination. Theor Popul Biol. 1983 Apr;23(2):183–201. [PubMed]
  • Hudson RR, Kaplan NL. The coalescent process in models with selection and recombination. Genetics. 1988 Nov;120(3):831–840. [PMC free article] [PubMed]
  • Hughes AL, Nei M. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature. 1988 Sep 8;335(6186):167–170. [PubMed]
  • Kusaba M, Nishio T, Satta Y, Hinata K, Ockendon D. Striking sequence similarity in inter- and intra-specific comparisons of class I SLG alleles from Brassica oleracea and Brassica campestris: implications for the evolution and recognition mechanism. Proc Natl Acad Sci U S A. 1997 Jul 8;94(14):7673–7678. [PMC free article] [PubMed]
  • May G, Shaw F, Badrane H, Vekemans X. The signature of balancing selection: fungal mating compatibility gene evolution. Proc Natl Acad Sci U S A. 1999 Aug 3;96(16):9172–9177. [PMC free article] [PubMed]
  • Richman AD, Kohn JR. Self-incompatibility alleles from Physalis: implications for historical inference from balanced genetic polymorphisms. Proc Natl Acad Sci U S A. 1999 Jan 5;96(1):168–172. [PMC free article] [PubMed]
  • Richman AD, Kao TH, Schaeffer SW, Uyenoyama MK. S-allele sequence diversity in natural populations of Solanum carolinense (Horsenettle). Heredity (Edinb) 1995 Oct;75(Pt 4):405–415. [PubMed]
  • Richman AD, Uyenoyama MK, Kohn JR. S-allele diversity in a natural population of Physalis crassifolia (Solanaceae) (ground cherry) assessed by RT-PCR. Heredity (Edinb) 1996 May;76(Pt 5):497–505. [PubMed]
  • Schierup MH, Hein J. Consequences of recombination on traditional phylogenetic analysis. Genetics. 2000 Oct;156(2):879–891. [PMC free article] [PubMed]
  • Schierup MH, Vekemans X, Christiansen FB. Evolutionary dynamics of sporophytic self-incompatibility alleles in plants. Genetics. 1997 Oct;147(2):835–846. [PMC free article] [PubMed]
  • Schierup MH, Vekemans X, Christiansen FB. Allelic genealogies in sporophytic self-incompatibility systems in plants. Genetics. 1998 Nov;150(3):1187–1198. [PMC free article] [PubMed]
  • Schierup MH, Mable BK, Awadalla P, Charlesworth D. Identification and characterization of a polymorphic receptor kinase gene linked to the self-incompatibility locus of Arabidopsis lyrata. Genetics. 2001 May;158(1):387–399. [PMC free article] [PubMed]
  • Seddon JM, Baverstock PR. Variation on islands: major histocompatibility complex (Mhc) polymorphism in populations of the Australian bush rat. Mol Ecol. 1999 Dec;8(12):2071–2079. [PubMed]
  • Awadalla P, Charlesworth D. Recombination and selection at Brassica self-incompatibility loci. Genetics. 1999 May;152(1):413–425. [PMC free article] [PubMed]
  • Takahata N. A simple genealogical structure of strongly balanced allelic lines and trans-species evolution of polymorphism. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2419–2423. [PMC free article] [PubMed]
  • Awadalla P, Eyre-Walker A, Smith JM. Linkage disequilibrium and recombination in hominid mitochondrial DNA. Science. 1999 Dec 24;286(5449):2524–2525. [PubMed]
  • Takahata N, Nei M. Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics. 1990 Apr;124(4):967–978. [PMC free article] [PubMed]
  • Ayala FJ. The myth of Eve: molecular biology and human origins. Science. 1995 Dec 22;270(5244):1930–1936. [PubMed]
  • Bergström TF, Josefsson A, Erlich HA, Gyllensten U. Recent origin of HLA-DRB1 alleles and implications for human evolution. Nat Genet. 1998 Mar;18(3):237–242. [PubMed]
  • Takahata N, Satta Y, Klein J. Polymorphism and balancing selection at major histocompatibility complex loci. Genetics. 1992 Apr;130(4):925–938. [PMC free article] [PubMed]
  • Casselman AL, Vrebalov J, Conner JA, Singhal A, Giovannoni J, Nasrallah ME, Nasrallah JB. Determining the physical limits of the Brassica S locus by recombinational analysis. Plant Cell. 2000 Jan;12(1):23–33. [PMC free article] [PubMed]
  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997 Dec 15;25(24):4876–4882. [PMC free article] [PubMed]
  • Wang X, Hughes AL, Tsukamoto T, Ando T, Kao T. Evidence that intragenic recombination contributes to allelic diversity of the S-RNase gene at the self-incompatibility (S) locus in Petunia inflata. Plant Physiol. 2001 Feb;125(2):1012–1022. [PMC free article] [PubMed]
  • Uyenoyama MK. Genealogical structure among alleles regulating self-incompatibility in natural populations of flowering plants. Genetics. 1997 Nov;147(3):1389–1400. [PMC free article] [PubMed]
  • Wiuf C, Hein J. On the number of ancestors to a DNA sequence. Genetics. 1997 Nov;147(3):1459–1468. [PMC free article] [PubMed]
  • Vekemans X, Slatkin M. Gene and allelic genealogies at a gametophytic self-incompatibility locus. Genetics. 1994 Aug;137(4):1157–1165. [PMC free article] [PubMed]
  • Wall JD. A comparison of estimators of the population recombination rate. Mol Biol Evol. 2000 Jan;17(1):156–163. [PubMed]

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