Skip to main content
Log in

Heterosynapsis and suppression of chiasmata within heterozygous pericentric inversions of the Sitka deer mouse

  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

The patterns of chromosomal pairing and chiasma distribution were analyzed in male Sitka deer mice (Peromyscus sitkensis) polymorphic for terminally positioned pericentric inversions of chromosomes 6 and 7. Gand C-banding of somatic metaphases indicated that the inversions involved 30% and 40% of chromosomes 6 and 7, respectively. Analysis of silver-stained synaptonemal complexes in surface-spread zygotene and pachytene nuclei from heterozygous individuals revealed that inversion loops were not formed. The inverted segments proceeded directly to heterosynapsis without an intervening homosynaptic phase, and the heteromorphic bivalents remained straight-paired throughout pachynema. C-banded pachytene nuclei corroborated the occurrence of heterosynapsis, as the heteromorphic bivalents exhibited nonaligned centromeres. Analysis of diplonema and diakinesis indicated that crossing over had not occurred within the heterosynapsed inverted segments. The observation of chiasma suppression within the inversions indicates that pericentric inversion heterozygosity does not lead to the production of unbalanced gametes. Heterosynapsis of the inverted segments during zygonema and pachynema and the resulting chiasma suppression therefore represent a meiotic mechanism for the maintenance of pericentric inversion polymorphisms in this population of P. sitkensis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ashley T, Moses MJ, Solari AJ (1981) Fine structure and behaviour of a pericentric inversion in the sand rat, Psammomys obesus. J Cell Sci 50:105–119

    Google Scholar 

  • Baker RJ, Gardner AL, Patton JL (1972) Chromosomal polymorphism in the phyllostomatid bat, Mimon crenulatum (Geoffroy). Experientia 28:969–970

    Google Scholar 

  • Bass RA (1979) Chromosomal polymorphism in cardinals Cardinalis cardinalis. Can J Genet Cytol 21:549–553

    Google Scholar 

  • Bitgood JJ, Shoffner RN, Otis JS, Wang N (1982) Recombinant inversion chromosomes in phenotypically normal chickens. Science 215:409–411

    Google Scholar 

  • Chandley AC (1982) A pachytene analysis of two male-fertile paracentric inversions in chromosome 1 of the mouse and in the male-sterile double heterozygote. Chromosoma 85:127–135

    Google Scholar 

  • Cole CJ (1970) Karyotypes and evolution of the spinosus group of lizards in the genus Sceloporus. Am Mus Novit 2431:1–47

    Google Scholar 

  • Committee for the Standardization of Chromosomes of Peromyscus (1977) Standardized karyotype of the deer mouse, Peromyscus (Rodentia). Cytogenet Cell Genet 19:38–43

    Google Scholar 

  • Counce CJ, Meyer GF (1973) Differentiation of the synaptonemal complex and the kinetochore in Locusta spermatocytes studied by whole mount electron microscopy. Chromosoma 44:231–253

    Google Scholar 

  • Davis KM, Smith SA, Greenbaum IF (1986) Evolutionary implications of chromosomal polymorphisms in Peromyscus boylii from southwestern Mexico. Evolution 40:645–649

    Google Scholar 

  • Davisson MT, Poorman PA, Roderick TH, Moses MJ (1981) A pericentric inversion in the mouse. Cytogenet Cell Genet 30:70–76

    Google Scholar 

  • Dobzhansky T (1970) Genetics of the evolutionary process. Columbia University Press, New York

    Google Scholar 

  • Dresser ME, Moses MJ (1980) Synaptonemal complex karyotyping in spermatocytes of the Chinese hamster (Cricetulus griseus): IV. Light and electron microscopy of synapsis and nucleolar development by silver staining. Chromosoma 76:1–22

    Google Scholar 

  • Elder FFB, Pathak S (1980) Light microscopic observations on the behavior of silver-stained trivalents in pachytene cells of Sigmodon fulviventer (Rodentia, Muridae) heterozygous for centric fusion. Cytogenet Cell Genet 27:31–38

    Google Scholar 

  • Greenbaum IF, Reed MJ (1984) Evidence for heterosynaptic pairing of the inverted segment in pericentric inversion heterozygotes of the deer mouse (Peromyscus maniculatus). Cytogenet Cell Genet 38:106–111

    Google Scholar 

  • Greenbaum IF, Baker RJ, Bowers JH (1978) Chromosomal homology and divergence between sibling species of deer mice: Peromyscus maniculatus and P. melanotis (Rodentia, Cricetidae). Evolution 32:334–341

    Google Scholar 

  • Greenbaum IF, Hale DW, Fuxa KP (1986a) The mechanism of autosomal synapsis and the substaging of zygonema and pachynema from deer mouse spermatocytes. Chromosoma 93:203–212

    Google Scholar 

  • Greenbaum IF, Hale DW, Fuxa KP (1986b) Synaptic adaptation in deer mice: A cellular mechanism for karyotypic orthoselection. Evolution 40:208–213

    Google Scholar 

  • Guichaoua MR, Delafontaine D, Taurelle R, Taillemite JL, Morazzani MR, Luciani JM (1986) Loop formation and synaptic adjustment in a human male heterozygous for two pericentric inversions. Chromosoma 93:313–320

    Google Scholar 

  • Gunn SJ, Greenbaum IF (1986) Systematic implications of karyotypic and morphologic variation in mainland Peromyscus from the Pacific Northwest. J Mammal 67:294–304

    Google Scholar 

  • Hale DW, Greenbaum IF (1986) The behavior and morphology of the X and Y chromosomes during prophase I in the Sitka deer mouse (Peromyscus sitkensis). Chromosoma 94:235–242

    Google Scholar 

  • Howell WM, Black DA (1980) Controlled silver staining of nucleolus organizer regions with a protective colloidal developer: A 1-step method. Experientia 36:1014–1015

    Google Scholar 

  • Kaelbling M, Fechheimer NS (1985) Synaptonemal complex analysis of a pericentric inversion in chromosome 2 of the domestic fowl, Gallus domesticus. Cytogenet Cell Genet 39:82–86

    Google Scholar 

  • Kaiser P (1984) Pericentric inversions: Problems and significance for clinical genetics. Hum Genet 68:1–47

    Google Scholar 

  • Lande R (1979) Effective deme sizes during long-term evolution estimated from rates of chromosomal rearrangement. Evolution 33:234–251

    Google Scholar 

  • Lande R (1984) The expected fixation rate of chromosomal inversions. Evolution 38:743–752

    Google Scholar 

  • Lee MR, Elder FFB (1980) Yeast stimulation of bone marrow mitosis for cytogenetic investigations. Cytogenet Cell Genet 26:36–40

    Google Scholar 

  • Mahadevaiah S, Mittwoch U, Moses MJ (1984) Pachytene chromosomes in male and female mice heterozygous for the Is(7; 1)4OH insertion. Chromosoma 90:163–169

    Google Scholar 

  • Mascarello JT, Warner JW (1974) Chromosome variations in the plains woodrat: A pericentric inversion involving constitutive heterochromatin. Experientia 30:90–91

    Google Scholar 

  • Matthey R (1966) Une inversion pericentrique a l'origine d'un polymorphisme chromosomique non-Robertsonien dans une population de Mastomys (Rodentia-Murinae). Chromosoma 18:188–200

    Google Scholar 

  • Moses MJ (1977) Synaptonemal complex karyotyping in spermatocytes of the Chinese hamster (Cricetulus griseus): I. Morphology of the autosomal complement in spread preparations. Chromosoma 60:99–125

    Google Scholar 

  • Moses MJ, Poorman PA (1981) Synaptonemal complex analysis of mouse chromosomal rearrangements: II. Synaptic adjustment in a tandem duplication. Chromosoma 81:519–535

    Google Scholar 

  • Moses MJ, Poorman PA (1984) Synapsis, synaptic adjustment and DNA synthesis in mouse oocytes. Chromosomes Today 8:90–103

    Google Scholar 

  • Moses MJ, Karatsis PA, Hamilton AE (1979) Synaptonemal complex analysis of heteromorphic trivalents in Lemur hybrids. Chromosoma 70:141–160

    Google Scholar 

  • Moses MJ, Poorman PA, Roderick TH, Davisson MT (1982) Synaptonemal complex analysis of mouse chromosomal rearrangements: IV. Synapsis and synaptic adjustment in two paracentric inversions. Chromosoma 84:457–474

    Google Scholar 

  • Ohno S, Weiler C, Poole J, Christian L, Stenius C (1966) Autosomal polymorphism due to pericentric inversions in the deer mouse (Peromyscus maniculatus) and some evidence of somatic segregation. Chromosoma 18:177–187

    Google Scholar 

  • Pengilly D, Jarrell GH, MacDonald SO (1983) Banded karyotypes of Peromyscus sitkensis from Baranof Island, Alaska. J Mammal 64:682–685

    Google Scholar 

  • Poorman PA, Moses MJ, Davisson MT, Roderick TH (1981) Synaptonemal complex analysis of mouse chromosomal rearrangements: III. Cytogenetic observations on two paracentric inversions. Chromosoma 83:419–429

    Google Scholar 

  • Roderick TH, Hawes NL (1974) Nineteen paracentric chromosomal inversions in mice. Genetics 76:109–117

    Google Scholar 

  • Rogers DS, Greenbaum IF, Gunn SJ, Engstrom MD (1984) Cytosystematic value of chromosomal inversion data in the genus Peromyscus (Rodentia: Cricetidae). J Mammal 65:457–465

    Google Scholar 

  • Seabright M (1971) A rapid banding technique for human chromosomes. Lancet ii:971–972

    Google Scholar 

  • Sharp PJ (1986) Synaptic adjustment at a C-band heterozygosity. Cytogenet Cell Genet 41:56–57

    Google Scholar 

  • Shields GF (1973) Chromosomal polymorphism common to several species of Junco (Aves). Can J Genet Cytol 15:461–471

    Google Scholar 

  • Shields GF (1976) Meiotic evidence for pericentric inversion polymorphism in Junco (Aves). Can J Genet Cytol 18:747–751

    Google Scholar 

  • Sites JW (1983) Chromosome evolution in the iguanid lizard Sceloporus grammicus. I. Chromosome polymorphisms. Evolution 37:38–53

    Google Scholar 

  • Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306

    Google Scholar 

  • Tease C, Fisher G (1986) Further examination of the production-line hypothesis in mouse foetal oocytes: I. Inversion heterozygotes. Chromosoma 93:447–452

    Google Scholar 

  • Thorneycroft HB (1975) A cytogenetic study of the white-throated sparrow, Zonotrichia albicollis (Gmelin). Evolution 29:611–621

    Google Scholar 

  • Turner BJ, Grudzien TA, Adkisson KP, Worrell RA (1985) Extensive chromosomal divergence within a single river basin in the goodeid fish, Ilyodon furcidens. Evolution 39:122–134

    Google Scholar 

  • White MJD (1973) Animal cytology and evolution. Cambridge University Press, London

    Google Scholar 

  • White MJD (1978) Modes of speciation. Freeman, San Francisco

    Google Scholar 

  • Yosida TH (1977) Frequencies of chromosome polymorphism in pairs no. 1, 9, and 13 in three geographical variants of black rats, Rattus rattus. Chromosoma 60:391–398

    Google Scholar 

  • Yosida TH, Tsuchiya K, Moriwaki K (1971) Frequency of chromosome polymorphism in Rattus rattus collected in Japan. Chromosoma 33:30–40

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hale, D.W. Heterosynapsis and suppression of chiasmata within heterozygous pericentric inversions of the Sitka deer mouse. Chromosoma 94, 425–432 (1986). https://doi.org/10.1007/BF00292751

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00292751

Keywords

Navigation