Abstract
The three chromosomal species of theMus terricolor complex possess 2n = 40 chromosomes. We show that their karyotypes differ in stable heterochromatin variations fixed in homozygous condition as prominent short arms in autosomes 1, 3 and 6. The three chromosomal species exhibit a high incidence of polymorphisms for Robertsonian fusions and pericentric inversions. Breeding experiments and histological analysis of testis show that heterozygosity for pericentric inversions and Robertsonian fusions had no effect on fertility. Meiotic analysis shows normal overall progression of meiosis in the heterozygotes, which is consistent with their normal gametogenesis. Nevertheless, both the inversion and fusion heterozygotes had undergone some alterations in the regular process of homologous synapsis, and it appeared that certain features of the meiotic system circumvented the potential negative effects of these polymorphic chromosomal rearrangements. The results indicate that the attributes of the meiotic system in a given organism could modulate the potential of a chromosomal rearrangement as reproductive barrier. The meiotic modulation hypothesis offers an explanation for the contradictory effects of the similar kinds of chromosomal mutations reported in different species.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bardhan A. and Sharma T. 2000 Sequential meiotic prophase development in pubertal Indian pygmy field mouse: Synaptic progression of the XY chromosomes, autosomal heterochromatin, and pericentric inversions.Genome 43, 172–180.
Batanian J. and Hulten M. 1987 Electron microscopic investigations of synaptonemal complexes in an infertile human male carrier of a pericentric inversion inv(1)(p32q42). Regular loop formation but defective synapsis including a possible inter-chromosomal effect.Hum. Genet. 76, 81–89.
Britton-Davidian J., Sonjaya H., Catalan J. and Cattaneo-Berrebi G. 1990 Robertsonian heterozygosity in wild mice: fertility and transmission rates in Rb(16.17) translocation heterozygotes.Genetica 80, 171–174.
Brown G. M., Leversha M., Hulten M., Ferguson-Smith M. A., Affara N. A. and Furlong R. A. 1998 Genetic analysis of meiotic recombination in humans by use of sperm typing: Reduced recombination within a heterozygous paracentric inversion of chromosome 9q32-q34.3.Am. J. Hum. Genet. 62, 1484–1492.
Committee on Standardized Genetic Nomenclature for Mice 1972 Standard karyotype of the mouse,Mus musculus. J. Hered. 63, 69–72.
Davis K. M., Smith S. A. and Greenbaum I. F. 1986 Evolutionary implications of chromosomal polymorphisms inPeromyscus boylii from southwestern Mexico.Evolution 40, 645–649.
Davisson M. T., Poorman P. A., Roderick T. H. and Moses M. J. 1981 A pericentric inversion in the mouse.Cytogenet. Cell Genet. 30, 70–76.
Dobson M. J., Pearlman R. E., Karaiskakis A., Spyropoulos B. and Moens P. 1994 Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction.J. Cell Sci. 107, 2749–2760.
Evans P. E., Breckon G. and Ford C. E. 1964 An air-drying method for meiotic preparations from mammalian testes.Cytogenetics 3, 289–294.
Fletcher J. M. 1979 Light microscopic analysis of meiotic prophase chromosomes by silver staining.Chromosoma 72, 241–248.
Forejt J. 1996 Hybrid sterility in the mouse.Trends Genet. 12, 412–417.
Fryns J. P., Haspeslagh M., Goodeeris P., Van Aerde J., Eggermont E. and Van Den Berghe H. 1981 Balanced and unbalanced pericentric inversion of chromosome 11.Ann. Genet. 24, 182–183.
Hale D. W. 1986 Heterosynapsis and suppression of chiasmata within heterozygous pericentric inversions of the Sitka deer mouse.Chromosoma 94, 425–432.
Hall W. P. 1983 Modes of speciation and evolution in the sceloporine iguanid lizards. I. Epistemology of the comparative approach and introduction to the problem. InAdvances in herpetology and evolutionary biology (ed. A. E. J. Rhodin and K. Myata), pp. 643–679. Museum of Comparative Zoology, Cambridge.
King M. 1981 Chromosome change and speciation in lizards. InEvolution and speciation (ed. W. R. Atchley and D. S. Woodruff), pp. 262–285. Cambridge University Press, Cambridge.
King M. 1993Species evolution: the role of chromosome change. Cambridge University Press, Cambridge.
Miklos G. L. G. 1974 Sex-chromosome pairing and male fertility.Cytogenet. Cell Genet. 13, 558–577.
Moses M. J., Karatsis P. A. and Hamilton A. C. 1979 Synaptonemal complex analysis of heteromorphic trivalents inLemur hybrids.Chromosoma 70, 141–160.
Moses M. J., Poorman P. A., Roderick T. H. and Davisson M. T. 1982 Synaptonemal complex analysis of mouse chromosomal rearrangements. II. Synapsis and synaptic adjustment in two paracentric inversions.Chromosoma 84, 454–474.
Nachman M. W. 1992 Meiotic studies of Robertsonian poly-morphisms in the South American marsh ratHolochilus brasiliensis.Cytogenet. Cell Genet. 61, 17–24.
Nachman M. W. and Myers P. 1989 Exceptional chromosomal mutations in a rodent population are not strongly underdominant.Proc. Natl. Acad. Sci. USA 86, 6666–6670.
Porter C. A. and Sites J. W. 1985 Normal disjunction in Robertsonian heterozygotes from a highly polymorphic lizard population.Cytogenet. Cell Genet. 39, 250–257.
Preito F., Badia L., Asensi F., Moya A. and Figuera M.-J. 1981 Pericentric inversions of chromosome 12 in two families.Hum. Genet. 57, 131–133.
Saitoh M. and Obara Y. 1988 Meiotic studies of interracial hybrids from the wild population of the large Japanese field mouse, Apodemus speciosus speciosus,Zool. Sci. 5, 815–822.
Seabright M. 1971 A rapid banding technique for human chromosomes.Lancet 2, 971–972.
Searle J. B. 1990 A cytogenetical analysis of reproduction in common shrews (Sorex araneus) from a karyotypic hybrid zone.Hereditas 113, 121–132.
Sen S. 1980 Cytogenetic investigations of some Indian rodents. Ph.D. thesis, Banaras Hindu University, Varanasi, India.
Sharma T. 1996 Chromosomal and molecular divergence in the Indian pygmy field miceMus booduga-terricolor lineage of the subgenus Mus.Genetica 97, 331–338.
Shaw D. D. 1981 Chromosomal hybrid zones in Orthopteroid insects. InEvolution and speciation (ed. W. R. Atchley and D.S. Woodruff), pp. 146–170. Cambridge University Press, Cambridge.
Speed R. M. 1986 Oocyte development in XO fetuses of man and mouse: the possible role of heterologous X-chromosome pairing in germ cell survival.Chromosoma 94, 115–124.
Stene J. and Stengel-Rutowski S. 1988 Genetic risks of familial reciprocal and Robertsonian translocation carriers. InThe cytogenetics of mammalian autosomal rearrangements (ed. A. Daniel), pp. 3–72. Alan R. Liss, New York.
Sumner A. T. 1972 A simple technique for demonstrating heterochromatin.Exp. Cell Res. 75, 304–306.
Tease C. and Fisher G. 1988. Chromosome pairing in foetal oocytes of mouse inversion heterozygotes. InKew chromosome conference III (ed. P. E. Brandham), pp. 293–298. Her Majesty’s Stationery Office, London.
Wallace B. M. N., Searle J. B. and Everret C. A. 1992 Male meiosis and gametogenesis in wild house mice (Mus musculus domesticus) from a chromosomal hybrid zone; a comparison between ’simple’ Robertsonian heterozygotes and homozygotes.Cytogenet. Cell Genet. 61, 211–220.
White M. J. D. 1973Animal cytology and evolution. Cambridge University Press, Cambridge.
White M. J. D. 1978Modes of speciation. Freeman, San Francisco.
White M. J. D. 1982 Rectangularity, speciation and chromosome architecture. InMechanisms of speciation (ed. C. Barigozzi), pp. 75–103. Alan R. Liss, New York.
Winsor E. J. T., Palmer C. G., Ellis P. M., Hunter J. L. P. and Ferguson-Smith M. A. 1978 Meiotic analysis of a pericentric inversion, inv(7)(p22q32), in the father of a child with duplication-deletion of chromosome 7.Cytogenet. Cell Genet. 20, 169–182.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Bardhan, A., Sharma, T. Meiosis and speciation: A study in a speciatingMus terricolor complex. J Genet 79, 105–111 (2000). https://doi.org/10.1007/BF02715858
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF02715858