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Genetics. Nov 2001; 159(3): 1179–1189.
PMCID: PMC1461872

Female meiosis drives karyotypic evolution in mammals.


Speciation is often accompanied by changes in chromosomal number or form even though such changes significantly reduce the fertility of hybrid intermediates. We have addressed this evolutionary paradox by expanding the principle that nonrandom segregation of chromosomes takes place whenever human or mouse females are heterozygous carriers of Robertsonian translocations, a common form of chromosome rearrangement in mammals. Our analysis of 1170 mammalian karyotypes provides strong evidence that karyotypic evolution is driven by nonrandom segregation during female meiosis. The pertinent variable in this form of meiotic drive is the presence of differing numbers of centromeres on paired homologous chromosomes. This situation is encountered in all heterozygous carriers of Robertsonian translocations. Whenever paired chromosomes have different numbers of centromeres, the inherent asymmetry of female meiosis and the polarity of the meiotic spindle dictate that the partner with the greater number of centromeres will attach preferentially to the pole that is most efficient at capturing centromeres. This mechanism explains how chromosomal variants become fixed in populations, as well as why closely related species often appear to have evolved by directional adjustment of the karyotype toward or away from a particular chromosome form. If differences in the ability of particular DNA sequences or chromosomal regions to function as centromeres are also considered, nonrandom segregation is likely to affect karyotype evolution across a very broad phylogenetic range.

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Selected References

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  • Adler ID, Johannisson R, Winking H. The influence of the Robertsonian translocation Rb(X.2)2Ad on anaphase I non-disjunction in male laboratory mice. Genet Res. 1989 Apr;53(2):77–86. [PubMed]
  • Agulnik SI, Agulnik AI, Ruvinsky AO. Meiotic drive in female mice heterozygous for the HSR inserts on chromosome 1. Genet Res. 1990 Apr;55(2):97–100. [PubMed]
  • Aranha IP, Martin-DeLeon PA. Segregation analysis of the mouse Rb(6.16) translocation in zygotes produced by heterozygous female carriers. Cytogenet Cell Genet. 1994;66(1):51–53. [PubMed]
  • Benirschke K, Rüedi D, Müller H, Kumamoto AT, Wagner KL, Downes HS. The unusual karyotype of the lesser kudu, Tragelaphus imberbis. Cytogenet Cell Genet. 1980;26(2-4):85–92. [PubMed]
  • Boué A, Boué J, Gropp A. Cytogenetics of pregnancy wastage. Adv Hum Genet. 1985;14:1–57. [PubMed]
  • Britton-Davidian J, Nadeau JH, Croset H, Thaler L. Genic differentiation and origin of Robertsonian populations of the house mouse (Mus musculus domesticus Rutty). Genet Res. 1989 Feb;53(1):29–44. [PubMed]
  • Britton-Davidian J, Sonjaya H, Catalan J, Cattaneo-Berrebi G. Robertsonian heterozygosity in wild mice: fertility and transmission rates in Rb(16.17) translocation heterozygotes. Genetica. 1990;80(3):171–174. [PubMed]
  • Britton-Davidian J, Catalan J, da Graça Ramalhinho M, Ganem G, Auffray JC, Capela R, Biscoito M, Searle JB, da Luz Mathias M. Rapid chromosomal evolution in island mice. Nature. 2000 Jan 13;403(6766):158–158. [PubMed]
  • Buckler ES, 4th, Phelps-Durr TL, Buckler CS, Dawe RK, Doebley JF, Holtsford TP. Meiotic drive of chromosomal knobs reshaped the maize genome. Genetics. 1999 Sep;153(1):415–426. [PMC free article] [PubMed]
  • Cano MI, Santos JL. Cytological basis of the B chromosome accumulation mechanism in the grasshopper Heteracris littoralis (Ramb). Heredity (Edinb) 1989 Feb;62(Pt 1):91–95. [PubMed]
  • Nachman MW, Boyer SN, Searle JB, Aquadro CF. Mitochondrial DNA variation and the evolution of Robertsonian chromosomal races of house mice, Mus domesticus. Genetics. 1994 Mar;136(3):1105–1120. [PMC free article] [PubMed]
  • Chayko CA, Martin-DeLeon PA. The murine Rb(6.16) translocation: alterations in the proportion of alternate sperm segregants effecting fertilization in vitro and in vivo. Hum Genet. 1992 Sep-Oct;90(1-2):79–85. [PubMed]
  • NOVITSKI E. Non-random disjunction in Drosophila. Genetics. 1951 May;36(3):267–280. [PMC free article] [PubMed]
  • NOVITSKI E. Genetic measures of centromere activity in Drosophila melanogaster. J Cell Physiol Suppl. 1955 May;45(Suppl 2):151–169. [PubMed]
  • Crow JF. A new study challenges the current belief of a high human male:female mutation ratio. Trends Genet. 2000 Dec;16(12):525–526. [PubMed]
  • Davisson MT, Akeson EC. Recombination suppression by heterozygous Robertsonian chromosomes in the mouse. Genetics. 1993 Mar;133(3):649–667. [PMC free article] [PubMed]
  • Pacchierotti F, Tiveron C, Mailhes JB, Davisson MT. Susceptibility to vinblastine-induced aneuploidy and preferential chromosome segregation during meiosis I in Robertsonian heterozygous mice. Teratog Carcinog Mutagen. 1995;15(5):217–230. [PubMed]
  • Dinkel BJ, O'Laughlin-Phillips EA, Fechheimer NS, Jaap RG. Gametic products transmitted by chickens heterozygous for chromosomal rearrangements. Cytogenet Cell Genet. 1979;23(1-2):124–136. [PubMed]
  • Page SL, Earnshaw WC, Choo KH, Shaffer LG. Further evidence that CENP-C is a necessary component of active centromeres: studies of a dic(X; 15) with simultaneous immunofluorescence and FISH. Hum Mol Genet. 1995 Feb;4(2):289–294. [PubMed]
  • Earnshaw WC, Ratrie H, 3rd, Stetten G. Visualization of centromere proteins CENP-B and CENP-C on a stable dicentric chromosome in cytological spreads. Chromosoma. 1989 Jun;98(1):1–12. [PubMed]
  • Pardo-Manuel de Villena F, Sapienza C. Nonrandom segregation during meiosis: the unfairness of females. Mamm Genome. 2001 May;12(5):331–339. [PubMed]
  • Evans EP, Lyon MF, Daglish M. A mouse translocation giving a metacentric marker chromosome. Cytogenetics. 1967;6(2):105–119. [PubMed]
  • Pardo-Manuel de Villena F, Sapienza C. Transmission ratio distortion in offspring of heterozygous female carriers of Robertsonian translocations. Hum Genet. 2001 Jan;108(1):31–36. [PubMed]
  • Everett CA, Searle JB. Pattern and frequency of nocodazole induced meiotic nondisjunction in oocytes of mice carrying the 'tobacco mouse' metacentric Rb(16.17)7Bnr. Genet Res. 1995 Aug;66(1):35–43. [PubMed]
  • Pardo-Manuel de Villena F, Sapienza C. Recombination is proportional to the number of chromosome arms in mammals. Mamm Genome. 2001 Apr;12(4):318–322. [PubMed]
  • Fredga K. Comparative chromosome studies in mongooses (Carnivora, Viverridae). I. Idiograms of 12 species and karyotype evolution in Herpestinae. Hereditas. 1972;71(1):1–74. [PubMed]
  • Pardo-Manuel de Villena F, de la Casa-Esperon E, Briscoe TL, Sapienza C. A genetic test to determine the origin of maternal transmission ratio distortion. Meiotic drive at the mouse Om locus. Genetics. 2000 Jan;154(1):333–342. [PMC free article] [PubMed]
  • Fuge H. Unorthodox male meiosis in Trichosia pubescens (Sciaridae). Chromosome elimination involves polar organelle degeneration and monocentric spindles in first and second division. J Cell Sci. 1994 Jan;107(Pt 1):299–312. [PubMed]
  • Peacock WJ, Dennis ES, Rhoades MM, Pryor AJ. Highly repeated DNA sequence limited to knob heterochromatin in maize. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4490–4494. [PMC free article] [PubMed]
  • Purvis A, Hector A. Getting the measure of biodiversity. Nature. 2000 May 11;405(6783):212–219. [PubMed]
  • Qumsiyeh MB. Evolution of number and morphology of mammalian chromosomes. J Hered. 1994 Nov-Dec;85(6):455–465. [PubMed]
  • Hamerton JL, Canning N, Ray M, Smith S. A cytogenetic survey of 14,069 newborn infants. I. Incidence of chromosome abnormalities. Clin Genet. 1975 Oct;8(4):223–243. [PubMed]
  • Harris MJ, Wallace ME, Evans EP. Aneuploidy in the embryonic progeny of females heterozygous for the Robertsonian chromosome (9.12) in genetically wild Peru-Coppock mice (Mus musculus). J Reprod Fertil. 1986 Jan;76(1):193–203. [PubMed]
  • Rhoades MM, Dempsey E. The Effect of Abnormal Chromosome 10 on Preferential Segregation and Crossing over in Maize. Genetics. 1966 May;53(5):989–1020. [PMC free article] [PubMed]
  • Rhoades MM, Vilkomerson H. On the Anaphase Movement of Chromosomes. Proc Natl Acad Sci U S A. 1942 Oct;28(10):433–436. [PMC free article] [PubMed]
  • Ruvinsky AO, Agulnik SI, Agulnik AI, Belyaev DK. The influence of mutations on chromosome 17 upon the segregation of homologues in female mice heterozygous for Robertsonian translocations. Genet Res. 1987 Dec;50(3):235–237. [PubMed]
  • Karpen GH, Allshire RC. The case for epigenetic effects on centromere identity and function. Trends Genet. 1997 Dec;13(12):489–496. [PubMed]
  • Sakurada K, Omoe K, Endo A. Increased incidence of unpartnered single chromatids in metaphase II oocytes in 39,X(XO) mice. Experientia. 1994 May 15;50(5):502–505. [PubMed]
  • Kaufman MH. Non-random segregation during mammalian oogenesis. Nature. 1972 Aug 25;238(5365):465–466. [PubMed]
  • Sánchez ER, Erickson RP. Wild-derived Robertsonian translocation in mice. Chromosome 17, Rb (16:17)7, shows novel interactions with t-alleles. J Hered. 1986 Sep-Oct;77(5):290–294. [PubMed]
  • LeMaire-Adkins R, Hunt PA. Nonrandom segregation of the mouse univalent X chromosome: evidence of spindle-mediated meiotic drive. Genetics. 2000 Oct;156(2):775–783. [PMC free article] [PubMed]
  • Sturtevant AH, Beadle GW. The Relations of Inversions in the X Chromosome of Drosophila Melanogaster to Crossing over and Disjunction. Genetics. 1936 Sep;21(5):554–604. [PMC free article] [PubMed]
  • Malik HS, Henikoff S. Adaptive evolution of Cid, a centromere-specific histone in Drosophila. Genetics. 2001 Mar;157(3):1293–1298. [PMC free article] [PubMed]
  • Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryder OA, O'Brien SJ. Molecular phylogenetics and the origins of placental mammals. Nature. 2001 Feb 1;409(6820):614–618. [PubMed]
  • Tease C, Fisher G. Two new X-autosome Robertsonian translocations in the mouse. I. Meiotic chromosome segregation in male hemizygotes and female heterozygotes. Genet Res. 1991 Oct;58(2):115–121. [PubMed]
  • Online access to trends in endocrinology and metabolism. Trends Endocrinol Metab. 1999 May;10(4):121–121. [PubMed]
  • Vassart M, Séguéla A, Hayes H. Chromosomal evolution in gazelles. J Hered. 1995 May-Jun;86(3):216–227. [PubMed]
  • Viroux MC, Bauchau V. Segregation and fertility in Mus musculus domesticus (wild mice) heterozygous for the Rb(4.12) translocation. Heredity (Edinb) 1992 Feb;68(Pt 2):131–134. [PubMed]

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