Skip to main content
Log in

MLH1-focus mapping in birds shows equal recombination between sexes and diversity of crossover patterns

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

Using immunolocalization of the mismatch-repair protein MLH1 in oocytes and spermatocytes of the Japanese quail and the zebra finch, we estimated the average amount of recombination in each sex of both species. In each case the number of MLH1 foci is statistically equivalent in males and females and the resulting sex-averaged map lengths are 2800 cM in the Japanese quail and 2275 cM in the zebra finch. In the Japanese quail the MLH1 foci are regularly distributed along the macrobivalents and recombination rates per Mb pair are somewhat lower compared to the chicken. In the zebra finch the MLH1 foci on the macrobivalents are substantially reduced in number relative to the Japanese quail and they show remarkable localization in both sexes. It is proposed that the lack of sex-dependent differences in recombination might be an extended feature among birds and that the different recombination patterns observed here reflect different controls of crossing over in spite of similarities regarding karyotypic asymmetry and DNA content. We discussed possible causes of the differences between birds and mammals, which show sex-dependent recombination differences.

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.

Institutional subscriptions

Similar content being viewed by others

References

  • Anderson LK, Reeves A, Webb LM, Ashley T (1999) Distribution of crossing over on mouse synaptonemal complexes using immunofluorescent localization of MLH1 protein. Genetics 151: 1569–1579.

    PubMed  CAS  Google Scholar 

  • Baker SM, Plug AW, Prolla TA et al. (1996) Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat Genet 13: 336–342.

    Article  PubMed  CAS  Google Scholar 

  • Barlow AL, Hultén MA (1998) Crossing over analysis at pachytene in man. Eur J Hum Genet 6: 350–358.

    Article  PubMed  CAS  Google Scholar 

  • Broman KW, Murray JC, Sheffield VC, White RL, Weber JL (1998) Comprehensive human genetic maps: individual and sex-specific variation in recombination. Am J Hum Genet 63: 861–869.

    Article  PubMed  CAS  Google Scholar 

  • Christidis L (1986) Chromosomal evolution within the family Estrildidae (Aves) I. The Poephilae. Genetica 71: 81–97.

    Article  Google Scholar 

  • Dietrich WF, Miller J, Steen R et al. (1996) A comprehensive genetic map of the mouse genome. Nature 380: 149–152.

    Article  PubMed  CAS  Google Scholar 

  • Dunzinger U, Nanda I, Schmid M, Haaf T, Zechner U (2005) Chicken orthologues of mammalian imprinted genes are clustered on macrochromosomes and replicate asynchronously. Trends Genet 21: 488–492.

    Article  PubMed  CAS  Google Scholar 

  • Froenicke L, Anderson LK, Wienberg J, Ashley T (2002) Male mouse recombination maps for each autosome identified by chromosome painting. Am J Hum Genet 71: 1353–1368.

    Article  PubMed  CAS  Google Scholar 

  • Hansson B, Akesson M, Slate J, Pemberton JM (2005) Linkage mapping reveals sex dimorphic map distances in a passerine bird. Proc Biol Sci 272: 2289–2298.

    Article  PubMed  CAS  Google Scholar 

  • Itoh Y, Arnold AP (2005) Chromosomal polymorphism and comparative painting analysis in the zebra finch. Chromosome Res 13: 47–56.

    Article  PubMed  CAS  Google Scholar 

  • Kaelbling M, Fechheimer NS (1983) Synaptonemal coplexes and the chromosome complement of domestic fowl Gallus domesticus. Cytogenet Cell Genet 35: 87–92.

    PubMed  CAS  Google Scholar 

  • Kayang BB, Vignal A, Inoue-Murayama M et al. (2004) A first-generation microsatellite linkage map of the Japanese quail. Anim Genet 35: 195–200.

    Article  PubMed  CAS  Google Scholar 

  • Kleckner N, Storlazzi A, Zickler D (2003) Coordinate variation in meiotic pachytene SC length and total crossover/chiasma frequency under conditions of constant DNA length. Trends Genet 9: 623–628.

    Article  CAS  Google Scholar 

  • Lenormand T (2003) The evolution of sex dimorphism in recombination. Genetics 163: 811–822.

    PubMed  Google Scholar 

  • Lynn A, Koehler KE, Judis L et al. (2002) Covariation of synaptonemal complex length and mammalian meiotic exchange rates. Science 296: 2222–2225.

    Article  PubMed  CAS  Google Scholar 

  • Paldi A, Gyapay G, Jami J (1995) Imprinted chromosomal regions of the human genome display sex-specific meiotic recombination frequencies. Current Biol 5: 1030–1035.

    Article  CAS  Google Scholar 

  • Pardo-Manuel de Villena F, Sapienza C (2001) Recombination is proportional to the number of chromosome arms in mammals. Mamm Genome 12: 318–322.

    Article  PubMed  CAS  Google Scholar 

  • Peterson DG, Stack SM, Healy JL, Donohoe BS, Anderson LK (1994) The relationship between synaptonemal complex length and genome size in four vertebrate classes (Osteicthyes, Reptilia, Aves, Mammalia). Chromosome Res 2: 153–162.

    Article  PubMed  CAS  Google Scholar 

  • Pigozzi MI (2001) Distribution of MLH1 foci on the synaptonemal complexes of chicken oocytes. Cytogenet Cell Genet 95: 129–133.

    Article  PubMed  CAS  Google Scholar 

  • Pigozzi MI, Solari AJ (1998) Germ cell restriction and regular transmission of an accessory chromosome that mimics a sex body in the zebra finch, Taeniopygia guttata. Chromosome Res 6: 105–113.

    Article  PubMed  CAS  Google Scholar 

  • Pigozzi MI, Solari AJ (1999a) Recombination nodule mapping and chiasma distribution in spermatocytes of the pigeon, Columba livia. Genome 42: 308–314.

    Article  PubMed  CAS  Google Scholar 

  • Pigozzi MI, Solari AJ (1999b) Equal frequencies of recombination nodules in both sexes of the pigeon suggest a basic difference with eutherian mammals. Genome 42: 315–321.

    Article  PubMed  CAS  Google Scholar 

  • Pigozzi MI, Solari AJ (2005) The germ-line-restricted chromosome in the zebra finch: recombination in females and elimination in males. Chromosoma 114: 403–409.

    Article  PubMed  CAS  Google Scholar 

  • Pollock DL, Fechheimer NS (1978) The chromosomes of cockerels (Gallus domesticus) during meiosis. Cytogenet Cell Genet 21: 267–281.

    PubMed  CAS  Google Scholar 

  • Quevedo C, del Cerro AL, Santos JL, Jones GH (1997) Correlated variation of chiasma frequency and synaptonemal complex length in Locusta migratoria. Heredity 78: 515–519.

    Article  Google Scholar 

  • Rahn MI, Solari AJ (1986) Recombination nodules in the oocytes of the chicken, Gallus domesticus. Cytogenet Cell Genet 43: 187–193.

    Article  PubMed  CAS  Google Scholar 

  • Reeves A (2001) MicroMeasure: a new computer program for the collection and analysis of cytogenetic data. Genome 44: 439–443.

    Article  PubMed  CAS  Google Scholar 

  • Rodionov AV, Chechik MS (2002) Lampbrush chromosomes in the Japanese quail Coturnix coturnix japonica: cytological maps of macro chromosomes and meiotic crossover frequency in females. Genetika 38: 1246–1251.

    PubMed  CAS  Google Scholar 

  • Rodionov AV, Chelysheva LA, Solovei IV, Miakoshina I (1992) Chiasma distribution in the lampbrush chromosomes of the chicken Gallus gallus domesticus: hot spots of recombination and their possible role in proper disjunction of homologous chromosomes at the first meiotic division. Genetika 28: 151–160.

    PubMed  CAS  Google Scholar 

  • Rodionov AV, Lukina NA, Galkina SA, Solovei I, Saccone S (2002) Crossing over in chicken oogenesis: cytological and chiasma-based genetic maps of the chicken lampbrush chromosome 1. J Hered 93: 125–129.

    Article  PubMed  CAS  Google Scholar 

  • Schmid M, Nanda I, Guttenbach M et al. (2000) First report on chicken genes and chromosomes. Cytogenet Cell Genet 90: 169–218.

    Article  PubMed  CAS  Google Scholar 

  • Sherman JD, Stack SM (1995) Two-dimensional spreads of synaptonemal complexes from solanaceous plants. VI. High-resolution recombination nodule map for tomato (Lycopersicon esculentum). Genetics 141: 683–708.

    PubMed  CAS  Google Scholar 

  • Shibusawa M, Minai S, Nishida-Umehara C et al. (2001) A comparative cytogenetic study of chromosome homology between chicken and Japanese quail. Cytogenet Cell Genet 95: 103–109.

    Article  PubMed  CAS  Google Scholar 

  • Solari AJ (1977) Ultrastructure of the synaptic autosome and the ZW bivalent in chicken oocytes. Chromosoma 64: 155–165.

    Article  Google Scholar 

  • Stock AD, Bunch TD (1982) The evolutionary implications of chromosome banding pattern homologies in the bird order Galliformes. Cytogenet Cell Genet 34: 136–148.

    PubMed  CAS  Google Scholar 

  • Takagi N (1972) A comparative study of the chromatin replication in 6 species of birds. Jpn J Genet 47: 115–123.

    Google Scholar 

  • Tease C, Hultén MA (2004) Inter-sex variation in synaptonemal complex lengths largely determine the different recombination rates in male and female germ cells. Cytogenet Genome Res 107: 208–215.

    Article  PubMed  CAS  Google Scholar 

  • Tease C, Hartshorne GM, Hultén MA (2002) Patterns of meiotic recombination in human fetal oocytes. Am J Hum Genet 70: 1469–1479.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. I. Pigozzi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Calderón, P.L., Pigozzi, M.I. MLH1-focus mapping in birds shows equal recombination between sexes and diversity of crossover patterns. Chromosome Res 14, 605–612 (2006). https://doi.org/10.1007/s10577-006-1059-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-006-1059-0

Key words

Navigation