Skip to main content
Genetics logoLink to Genetics
. 1997 Jul;146(3):1019–1034. doi: 10.1093/genetics/146.3.1019

Discordant Phylogeographic Patterns between the Y Chromosome and Mitochondrial DNA in the House Mouse: Selection on the Y Chromosome?

S Boissinot 1, P Boursot 1
PMCID: PMC1208032  PMID: 9215905

Abstract

We have compared patterns of geographic variation and molecular divergence of mitochondrial DNA (mtDNA) and Y chromosome over the range of the different subspecies of Mus musculus. MtDNA was typed for 305 nucleotides in the control region, the Y chromosome for 834 base pairs (bp) in Zfy introns and 242 bp in Sry, a Zfy2 18-bp deletion, and two microsatellites. Apparent discrepancies exist between the distributions of the lineages of mtDNA and of the two major Y-chromosome lineages thus defined: some subspecies share the same mtDNA lineage but have different Y-chromosome lineages or vice versa. One microsatellite reveals a geographically clustered variation inside the distribution of each Y-chromosome lineage, showing that new Y-chromosome variants can rapidly spread locally. The two major Y-chromosome lineages have a divergence time only about one fourth of that between mtDNA lineages. Although this recent coalescence of the Y chromosomes between subspecies could partly be due to a lower ancestral polymorphism of the Y chromosome, it suggests that secondary introgression after the radiation of the subspecies might have occurred. There is evidence that the differentiation of the Y-chromosome lineages contributes to partial reproductive isolation between subspecies, and patterns of molecular evolution suggest that selection has played a role in the rapid spread across subspecies.

Full Text

The Full Text of this article is available as a PDF (1.5 MB).

Selected References

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

  1. Bibb M. J., Van Etten R. A., Wright C. T., Walberg M. W., Clayton D. A. Sequence and gene organization of mouse mitochondrial DNA. Cell. 1981 Oct;26(2 Pt 2):167–180. doi: 10.1016/0092-8674(81)90300-7. [DOI] [PubMed] [Google Scholar]
  2. Bishop C. E., Boursot P., Baron B., Bonhomme F., Hatat D. Most classical Mus musculus domesticus laboratory mouse strains carry a Mus musculus musculus Y chromosome. Nature. 1985 May 2;315(6014):70–72. doi: 10.1038/315070a0. [DOI] [PubMed] [Google Scholar]
  3. Boursot P., Yonekawa H., Bonhomme F. Heteroplasmy in mice with deletion of a large coding region of mitochondrial DNA. Mol Biol Evol. 1987 Jan;4(1):46–55. doi: 10.1093/oxfordjournals.molbev.a040421. [DOI] [PubMed] [Google Scholar]
  4. Carlisle C., Winking H., Weichenhan D., Nagamine C. M. Absence of correlation between Sry polymorphisms and XY sex reversal caused by the M. m. domesticus Y chromosome. Genomics. 1996 Apr 1;33(1):32–45. doi: 10.1006/geno.1996.0156. [DOI] [PubMed] [Google Scholar]
  5. Chang B. H., Li W. H. Estimating the intensity of male-driven evolution in rodents by using X-linked and Y-linked Ube 1 genes and pseudogenes. J Mol Evol. 1995 Jan;40(1):70–77. doi: 10.1007/BF00166597. [DOI] [PubMed] [Google Scholar]
  6. Chang B. H., Shimmin L. C., Shyue S. K., Hewett-Emmett D., Li W. H. Weak male-driven molecular evolution in rodents. Proc Natl Acad Sci U S A. 1994 Jan 18;91(2):827–831. doi: 10.1073/pnas.91.2.827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Charlesworth B., Coyne J. A., Orr H. A. Meiotic drive and unisexual hybrid sterility: a comment. Genetics. 1993 Feb;133(2):421–432. doi: 10.1093/genetics/133.2.421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Conway S. J., Mahadevaiah S. K., Darling S. M., Capel B., Rattigan A. M., Burgoyne P. S. Y353/B: a candidate multiple-copy spermiogenesis gene on the mouse Y chromosome. Mamm Genome. 1994 Apr;5(4):203–210. doi: 10.1007/BF00360546. [DOI] [PubMed] [Google Scholar]
  9. Coward P., Nagai K., Chen D., Thomas H. D., Nagamine C. M., Lau Y. F. Polymorphism of a CAG trinucleotide repeat within Sry correlates with B6.YDom sex reversal. Nat Genet. 1994 Mar;6(3):245–250. doi: 10.1038/ng0394-245. [DOI] [PubMed] [Google Scholar]
  10. Graven L., Passarino G., Semino O., Boursot P., Santachiara-Benerecetti S., Langaney A., Excoffier L. Evolutionary correlation between control region sequence and restriction polymorphisms in the mitochondrial genome of a large Senegalese Mandenka sample. Mol Biol Evol. 1995 Mar;12(2):334–345. doi: 10.1093/oxfordjournals.molbev.a040206. [DOI] [PubMed] [Google Scholar]
  11. Guo S. W., Thompson E. A. Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics. 1992 Jun;48(2):361–372. [PubMed] [Google Scholar]
  12. Hammer M. F. A recent common ancestry for human Y chromosomes. Nature. 1995 Nov 23;378(6555):376–378. doi: 10.1038/378376a0. [DOI] [PubMed] [Google Scholar]
  13. Hammer M. F., Silver L. M. Phylogenetic analysis of the alpha-globin pseudogene-4 (Hba-ps4) locus in the house mouse species complex reveals a stepwise evolution of t haplotypes. Mol Biol Evol. 1993 Sep;10(5):971–1001. doi: 10.1093/oxfordjournals.molbev.a040051. [DOI] [PubMed] [Google Scholar]
  14. Hudson R. R. Gene trees, species trees and the segregation of ancestral alleles. Genetics. 1992 Jun;131(2):509–513. doi: 10.1093/genetics/131.2.509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hudson R. R., Kreitman M., Aguadé M. A test of neutral molecular evolution based on nucleotide data. Genetics. 1987 May;116(1):153–159. doi: 10.1093/genetics/116.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hurst L. D. Embryonic growth and the evolution of the mammalian Y chromosome. I. The Y as an attractor for selfish growth factors. Heredity (Edinb) 1994 Sep;73(Pt 3):223–232. doi: 10.1038/hdy.1994.127. [DOI] [PubMed] [Google Scholar]
  17. Hurst L. D., Pomiankowski A. Causes of sex ratio bias may account for unisexual sterility in hybrids: a new explanation of Haldane's rule and related phenomena. Genetics. 1991 Aug;128(4):841–858. doi: 10.1093/genetics/128.4.841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kaplan N. L., Hudson R. R., Langley C. H. The "hitchhiking effect" revisited. Genetics. 1989 Dec;123(4):887–899. doi: 10.1093/genetics/123.4.887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Koopman P., Gubbay J., Collignon J., Lovell-Badge R. Zfy gene expression patterns are not compatible with a primary role in mouse sex determination. Nature. 1989 Dec 21;342(6252):940–942. doi: 10.1038/342940a0. [DOI] [PubMed] [Google Scholar]
  20. Milishnikov A. N., Rafiev A. N., Lavrenchenko L. A., Orlov V. N. Vysokii uroven' introgressii genov Mus domesticus v populiatsii Mus musculus s. str. Zakavkaz'ia. Dokl Akad Nauk SSSR. 1990;311(3):764–768. [PubMed] [Google Scholar]
  21. Miller K. E., Lundrigan B. L., Tucker P. K. Length variation of CAG repeats in Sry across populations of Mus domesticus. Mamm Genome. 1995 Mar;6(3):206–208. doi: 10.1007/BF00293015. [DOI] [PubMed] [Google Scholar]
  22. Miyata T., Hayashida H., Kuma K., Mitsuyasu K., Yasunaga T. Male-driven molecular evolution: a model and nucleotide sequence analysis. Cold Spring Harb Symp Quant Biol. 1987;52:863–867. doi: 10.1101/sqb.1987.052.01.094. [DOI] [PubMed] [Google Scholar]
  23. Morita T., Kubota H., Murata K., Nozaki M., Delarbre C., Willison K., Satta Y., Sakaizumi M., Takahata N., Gachelin G. Evolution of the mouse t haplotype: recent and worldwide introgression to Mus musculus. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):6851–6855. doi: 10.1073/pnas.89.15.6851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Moriwaki K., Yonekawa H., Gotoh O., Minezawa M., Winking H., Gropp A. Implications of the genetic divergence between European wild mice with Robertsonian translocations from the viewpoint of mitochondrial DNA. Genet Res. 1984 Jun;43(3):277–287. doi: 10.1017/s0016672300026069. [DOI] [PubMed] [Google Scholar]
  25. Nachman M. W., Aquadro C. F. Polymorphism and divergence at the 5' flanking region of the sex-determining locus, Sry, in mice. Mol Biol Evol. 1994 May;11(3):539–547. doi: 10.1093/oxfordjournals.molbev.a040133. [DOI] [PubMed] [Google Scholar]
  26. Nagamine C. M., Nishioka Y., Moriwaki K., Boursot P., Bonhomme F., Lau Y. F. The musculus-type Y chromosome of the laboratory mouse is of Asian origin. Mamm Genome. 1992;3(2):84–91. doi: 10.1007/BF00431251. [DOI] [PubMed] [Google Scholar]
  27. Nagamine C. M., Shiroishi T., Miyashita N., Tsuchiya K., Ikeda H., Takao N., Wu X. L., Jin M. L., Wang F. S., Kryukov A. P. Distribution of the molossinus allele of Sry, the testis-determining gene, in wild mice. Mol Biol Evol. 1994 Nov;11(6):864–874. doi: 10.1093/oxfordjournals.molbev.a040169. [DOI] [PubMed] [Google Scholar]
  28. Nei M., Miller J. C. A simple method for estimating average number of nucleotide substitutions within and between populations from restriction data. Genetics. 1990 Aug;125(4):873–879. doi: 10.1093/genetics/125.4.873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Nishioka Y., Dolan B. M., Prado V. F., Zahed L., Tyson H. Comparison of mouse Y-chromosomal repetitive sequences isolated from Mus musculus, M. spicilegus, and M. spretus. Cytogenet Cell Genet. 1993;64(1):54–58. doi: 10.1159/000133560. [DOI] [PubMed] [Google Scholar]
  30. Nishioka Y., Dolan B. M., Zahed L., Prado V., Tyson H. Molecular evolution of a Y-chromosomal repetitive sequence family in the genus Mus. Mol Biol Evol. 1994 Jan;11(1):146–153. doi: 10.1093/oxfordjournals.molbev.a040083. [DOI] [PubMed] [Google Scholar]
  31. Nishioka Y. Y-chromosomal DNA polymorphism in mouse inbred strains. Genet Res. 1987 Aug;50(1):69–72. doi: 10.1017/s0016672300023351. [DOI] [PubMed] [Google Scholar]
  32. Orth A., Lyapunova E., Kandaurov A., Boissinot S., Boursot P., Vorontsov N., Bonhomme F. L'espèce polytypique Mus musculus en Transcaucasie. C R Acad Sci III. 1996 May;319(5):435–441. [PubMed] [Google Scholar]
  33. Prager E. M., Tichy H., Sage R. D. Mitochondrial DNA sequence variation in the eastern house mouse, Mus musculus: comparison with other house mice and report of a 75-bp tandem repeat. Genetics. 1996 May;143(1):427–446. doi: 10.1093/genetics/143.1.427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Rice W. R. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature. 1996 May 16;381(6579):232–234. doi: 10.1038/381232a0. [DOI] [PubMed] [Google Scholar]
  35. Shimmin L. C., Chang B. H., Li W. H. Male-driven evolution of DNA sequences. Nature. 1993 Apr 22;362(6422):745–747. doi: 10.1038/362745a0. [DOI] [PubMed] [Google Scholar]
  36. Silver L. M., Hammer M., Fox H., Garrels J., Bucan M., Herrmann B., Frischauf A. M., Lehrach H., Winking H., Figueroa F. Molecular evidence for the rapid propagation of mouse t haplotypes from a single, recent, ancestral chromosome. Mol Biol Evol. 1987 Sep;4(5):473–482. doi: 10.1093/oxfordjournals.molbev.a040457. [DOI] [PubMed] [Google Scholar]
  37. Silver L. M. Mouse t haplotypes. Annu Rev Genet. 1985;19:179–208. doi: 10.1146/annurev.ge.19.120185.001143. [DOI] [PubMed] [Google Scholar]
  38. Silver L. M. The peculiar journey of a selfish chromosome: mouse t haplotypes and meiotic drive. Trends Genet. 1993 Jul;9(7):250–254. doi: 10.1016/0168-9525(93)90090-5. [DOI] [PubMed] [Google Scholar]
  39. Smith J. M., Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed] [Google Scholar]
  40. Suzuki H., Moriwaki K., Sakurai S. Sequences and evolutionary analysis of mouse 5S rDNAs. Mol Biol Evol. 1994 Jul;11(4):704–710. doi: 10.1093/oxfordjournals.molbev.a040149. [DOI] [PubMed] [Google Scholar]
  41. Tucker P. K., Lee B. K., Eicher E. M. Y chromosome evolution in the subgenus Mus (genus Mus). Genetics. 1989 May;122(1):169–179. doi: 10.1093/genetics/122.1.169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Tucker P. K., Lee B. K., Lundrigan B. L., Eicher E. M. Geographic origin of the Y chromosomes in "old" inbred strains of mice. Mamm Genome. 1992;3(5):254–261. doi: 10.1007/BF00292153. [DOI] [PubMed] [Google Scholar]
  43. Tucker P. K., Lundrigan B. L. The nature of gene evolution on the mammalian Y chromosome: lessons from Sry. Philos Trans R Soc Lond B Biol Sci. 1995 Nov 29;350(1333):221–227. doi: 10.1098/rstb.1995.0155. [DOI] [PubMed] [Google Scholar]
  44. Turelli M., Orr H. A. The dominance theory of Haldane's rule. Genetics. 1995 May;140(1):389–402. doi: 10.1093/genetics/140.1.389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Vanlerberghe F., Dod B., Boursot P., Bellis M., Bonhomme F. Absence of Y-chromosome introgression across the hybrid zone between Mus musculus domesticus and Mus musculus musculus. Genet Res. 1986 Dec;48(3):191–197. doi: 10.1017/s0016672300025003. [DOI] [PubMed] [Google Scholar]
  46. Whitfield L. S., Sulston J. E., Goodfellow P. N. Sequence variation of the human Y chromosome. Nature. 1995 Nov 23;378(6555):379–380. doi: 10.1038/378379a0. [DOI] [PubMed] [Google Scholar]
  47. Wu C. I. Inferences of species phylogeny in relation to segregation of ancient polymorphisms. Genetics. 1991 Feb;127(2):429–435. doi: 10.1093/genetics/127.2.429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Yonekawa H., Moriwaki K., Gotoh O., Miyashita N., Matsushima Y., Shi L. M., Cho W. S., Zhen X. L., Tagashira Y. Hybrid origin of Japanese mice "Mus musculus molossinus": evidence from restriction analysis of mitochondrial DNA. Mol Biol Evol. 1988 Jan;5(1):63–78. doi: 10.1093/oxfordjournals.molbev.a040476. [DOI] [PubMed] [Google Scholar]
  49. Zambrowicz B. P., Findley S. D., Simpson E. M., Page D. C., Palmiter R. D. Characterization of the murine Zfy1 and Zfy2 promoters. Genomics. 1994 Nov 15;24(2):406–408. doi: 10.1006/geno.1994.1641. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES