Skip to main content
SpringerLink
Log in

Genetic differentiation within and away from the chromosomal rearrangements characterising hybridising chromosomal races of the western house mouse (Mus musculus domesticus)

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

The importance of chromosomal rearrangements for speciation can be inferred from studies of genetic exchange between hybridising chromosomal races within species. Reduced fertility or recombination suppression in karyotypic hybrids has the potential to maintain or promote genetic differentiation in genomic regions near rearrangement breakpoints. We studied genetic exchange between two hybridising groups of chromosomal races of house mouse in Upper Valtellina (Lombardy, Italy), using microsatellites. These groups differ by Robertsonian fusions and/or whole-arm reciprocal translocations such that F1 hybrids have a chain-of-five meiotic configuration. Previous studies showed genetic differentiation in two chromosomes in the chain-of-five (10 and 12) close to their centromeres (i.e. the rearrangement breakpoints); we have shown here that the centromeric regions of the other two chromosomes in the chain (2 and 8) are similarly differentiated. The internal chromosomes of the chain (8 and 12) show the greatest differentiation, which may reflect pairing and recombination properties of internal and external elements in a meiotic chain. Importantly, we found that centromeric regions of some non-rearranged chromosomes also showed genetic differentiation between the hybridising groups, indicating a complex interplay between chromosomal rearrangements and other parts of the genome in maintaining or promoting differentiation and potentially driving speciation between chromosomal races.

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

Access this article

Log in via an institution

Price includes VAT (Finland)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

CHPO:

Poschiavo chromosomal race of the house mouse

cM:

centiMorgan

F CT :

Among group fixation index

ILVA:

Lower Valtellina chromosomal race of the house mouse

IMVA:

Mid Valtellina chromosomal race of the house mouse

IUVA:

Upper Valtellina chromosomal race of the house mouse

References

  • Barton NH, Hewitt GM (1985) Analysis of hybrid zones. Annu Rev Ecol Syst 16:113–148

    Article  Google Scholar 

  • Bidau CJ (1990) The complex Robertsonian system of Dichroplus pratensis (Melanoplinae, Acrididae). II. Effects of the fusion polymorphisms on chiasma frequency and distribution. Heredity 64:145–159

    Article  Google Scholar 

  • Bidau CJ, Giménez MD, Palmer CL, Searle JB (2001) The effects of Robertsonian fusions on chiasma frequency and distribution in the house mouse (Mus musculus domesticus) from a hybrid zone in northern Scotland. Heredity 87:305–313

    Article  CAS  PubMed  Google Scholar 

  • Brown JD, O’Neill RJ (2010) Chromosomes, conflict, and epigenetics: chromosomal speciation revisited. Annu Rev Genomics Hum Genet 11:291–316

    Article  CAS  PubMed  Google Scholar 

  • Chmátal L, Gabriel SI, Mitsainas GP et al (2014) Centromere strength provides the cell biological basis for meiotic drive and karyotype evolution in mice. Curr Biol 24:2295–3000

    Article  PubMed  PubMed Central  Google Scholar 

  • Colombo PC (1993) A polymorphic centric fusion enhances chiasma interference in a grasshopper: a chiasma distribution approach. Heredity 70:254–265

    Article  Google Scholar 

  • Daniel A (ed) (1988) The cytogenetics of mammalian autosomal rearrangements. Alan R Liss, New York

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Dumas D, Britton-Davidian J (2002) Chromosomal rearrangements and evolution of recombination: comparison of chiasma distribution patterns in standard and Robertsonian populations of the house mouse. Genetics 162:1355–1366

    PubMed  PubMed Central  Google Scholar 

  • Endler JA (1977) Geographic variation, speciation and clines. Princeton University Press, Princeton

    Google Scholar 

  • Epstein CJ (1986) The consequences of chromosome imbalance: principles, mechanisms, and models. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver. 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Faria R, Navarro A (2010) Chromosomal speciation revisited: rearranging theory with pieces of evidence. Trends Ecol Evol 25:660–669

    Article  PubMed  Google Scholar 

  • Feder JL, Egan SP, Nosil P (2012) The genomics of speciation-with-gene-flow. Trends Genet 28:342–350

    Article  CAS  PubMed  Google Scholar 

  • Ford CE, Evans EP (1973) Robertsonian translocations in mice: segregational irregularities in male heterozygotes and zygotic unbalance. Chrom Today 4:387–397

    Google Scholar 

  • Förster DW, Mathias ML, Britton-Davidian J, Searle JB (2013) Origin of the chromosomal radiation of Madeiran house mice: a microsatellite analysis of metacentric chromosomes. Heredity 110:380–388

    Article  PubMed  PubMed Central  Google Scholar 

  • Franchini P, Colangelo P, Solano E, Capanna E, Verheyen E, Castiglia R (2010) Reduced gene flow at pericentromeric loci in a hybrid zone involving chromosomal races of the house mouse Mus musculus domesticus. Evolution 64:2020–2032

    PubMed  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Garagna S, Page J, Fernandez-Donoso R, Zuccotti M, Searle JB (2014) The Robertsonian phenomenon in the house mouse: mutation, meiosis and speciation. Chromosoma 123:529–544

    Article  PubMed  Google Scholar 

  • Garrigan D, Kingan SB, Geneva AJ, Vedanayagam JP, Presgraves DC (2014) Genome diversity and divergence in Drosophila mauritiana: multiple signatures of faster X evolution. Genome Biol Evol 6:2444–2458

    Article  PubMed  PubMed Central  Google Scholar 

  • Giménez MD, White TA, Hauffe HC, Panithanarak T, Searle JB (2013) Understanding the basis of diminished gene flow between hybridizing chromosome races of the house mouse. Evolution 67:1446–1462

    PubMed  Google Scholar 

  • Hale DW (1986) Heterosynapsis and suppression of chiasmata within heterozygous pericentric inversions of the Sitka deer mouse. Chromosoma 94:425–432

    Article  CAS  PubMed  Google Scholar 

  • Harrison RG (1990) Hybrid zones: windows on the evolutionary process. Oxf Surv Evol Biol 7:69–128

    Google Scholar 

  • Hauffe HC, Searle JB (1993) Extreme karyotypic variation in a Mus musculus domesticus hybrid zone: the tobacco mouse story revisited. Evolution 47:1374–1395

    Article  Google Scholar 

  • Hauffe HC, Searle JB (1998) Chromosomal heterozygosity and fertility in house mice (Mus musculus domesticus) from northern Italy. Genetics 150:1143–1154

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hauffe HC, Panithanarak T, Dallas JF, Piálek J, Gündüz I, Searle JB (2004) The tobacco mouse and its relatives: a “tail” of coat colors, chromosomes, hybridization and speciation. Cytogenet Genome Res 105:395–405

    Article  CAS  PubMed  Google Scholar 

  • Hauffe HC, Giménez MD, Searle JB (2012) Chromosomal hybrid zones in the house mouse. In: Macholán M, Baird SJE, Munclinger P, Piálek J (eds) Evolution in the house mouse. Cambridge University Press, Cambridge, pp 407–430

    Chapter  Google Scholar 

  • King M (1993) Species evolution: the role of chromosome change. Cambridge University Press, Cambridge

    Google Scholar 

  • Matveevsky SN, Pavlova SV, Acaeva MM, Kolomiets OL (2012) Synaptonemal complex analysis of interracial hybrids between the Moscow and Neroosa chromosomal races of the common shrew Sorex araneus showing regular formation of a complex meiotic configuration (ring-of-four). Comp Cytogenet 6:301–314

    Article  PubMed  PubMed Central  Google Scholar 

  • Merico V, Giménez MD, Vasco C et al (2013) Chromosomal speciation in mice: a cytogenetic analysis of recombination. Chromosom Res 21:523–533

    Article  CAS  Google Scholar 

  • Nachman MW, Payseur BA (2012) Recombination rate variation and speciation: theoretical predictions and empirical results from rabbits and mice. Philos Trans R Soc B 367:409–421

    Article  Google Scholar 

  • Niehuis O, Gibson JD, Rosenberg MS et al (2010) Recombination and its impact on the genome of the haplodiploid parasitoid wasp Nasonia. PLoS ONE 5, e8597

    Article  PubMed  PubMed Central  Google Scholar 

  • Oka A, Shiroishi T (2012) The role of the X chromosome in house mouse speciation. In: Macholán M, Baird SJE, Munclinger P, Piálek J (eds) Evolution of the house mouse. Cambridge University Press, Cambridge, pp 431–454

    Chapter  Google Scholar 

  • Panithanarak T, Hauffe HC, Dallas JF, Glover A, Ward RG, Searle JB (2004) Linkage-dependent gene flow in a house mouse chromosomal hybrid zone. Evolution 58:184–192

    Article  PubMed  Google Scholar 

  • Piálek J, Hauffe HC, Rodríguez-Clark KM, Searle JB (2001) Raciation and speciation in house mice from the Alps: the role of chromosomes. Mol Ecol 10:613–625

    Article  PubMed  Google Scholar 

  • Rieseberg LH (2001) Chromosomal rearrangements and speciation. Trends Ecol Evol 16:351–358

    Article  PubMed  Google Scholar 

  • Searle JB (1993) Chromosomal hybrid zones in eutherian mammals. In: Harrison RG (ed) Hybrid zones and the evolutionary process. Oxford University Press, New York, pp 309–353

    Google Scholar 

  • Turner JMA, Mahadevaiah SK, Fernandez-Capetillo O et al (2005) Silencing of unsynapsed meiotic chromosomes in the mouse. Nat Genet 37:41–47

    CAS  PubMed  Google Scholar 

  • Weetman D, Wilding CS, Steen K, Pinto J, Donnelly MJ (2012) Gene flow-dependent genomic divergence between Anopheles gambiae M and S forms. Mol Biol Evol 29:279–291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank Soraia Barbosa, Alex Gomez Lepiz and Tom White for their assistance with the AMOVA. We are very grateful to Cassandra Ramirez for drawing the map. We would also like to thank the two anonymous reviewers for their valuable comments that improved the manuscript. Funding was provided by the Natural Environment Research Council (UK).

Author information

Authors and Affiliations

  1. Department of Biology, University of York, Wentworth Way, York, YO10 5DD, UK

    Daniel W. Förster, Eleanor P. Jones, Fríða Jóhannesdóttir, Sofia I. Gabriel, Mabel D. Giménez, Heidi C. Hauffe & Jeremy B. Searle

  2. Department of Evolutionary Genetics, Leibniz-Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str.17, 10315, Berlin, Germany

    Daniel W. Förster

  3. Fera Science, Sand Hutton, York, YO41 1LZ, UK

    Eleanor P. Jones

  4. Department of Ecology and Genetics, Uppsala University, Norbyv 18 D, 752 36, Uppsala, Sweden

    Fríða Jóhannesdóttir

  5. Department of Ecology and Evolution, Corson Hall, Cornell University, Ithaca, NY, 14853-2701, USA

    Fríða Jóhannesdóttir & Jeremy B. Searle

  6. CESAM – Centre for Environmental and Marine Studies, Departamento de Biologia Animal, Faculdade de Ciências da Universidade de Lisboa, 1749-016, Lisbon, Portugal

    Sofia I. Gabriel

  7. Instituto de Biología Subtropical, Facultad de Ciencias Exactas, Químicas y Naturales, Universidad Nacional de Misiones, Félix de Azara 1552, N3300LQH, Posadas, Misiones, Argentina

    Mabel D. Giménez

  8. Institute of Marine Science, Burapha University, Chonburi, Thailand

    Thadsin Panithanarak

  9. Department of Biodiversity and Molecular Ecology, Research and Innovation Centre, Fondazione Edmund Mach, Via E. Mach 1, 38010 S, Michele all’Adige, TN, Italy

    Heidi C. Hauffe

Authors
  1. Daniel W. Förster
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eleanor P. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fríða Jóhannesdóttir
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sofia I. Gabriel
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mabel D. Giménez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Thadsin Panithanarak
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Heidi C. Hauffe
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jeremy B. Searle
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jeremy B. Searle.

Ethics declarations

Ethical standards

All institutional and national guidelines for the care and use of field-collected and laboratory-maintained animals were followed.

Conflict of interest

The authors declare that they have no competing interests.

Additional information

Responsible Editor: Fengtang Yang

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(XLS 90 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Förster, D.W., Jones, E.P., Jóhannesdóttir, F. et al. Genetic differentiation within and away from the chromosomal rearrangements characterising hybridising chromosomal races of the western house mouse (Mus musculus domesticus). Chromosome Res 24, 271–280 (2016). https://doi.org/10.1007/s10577-016-9520-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-016-9520-1

Keywords

Search

Navigation