Original Article

Patterns of genic diversity and structure in a species undergoing rapid chromosomal radiation: an allozyme analysis of house mice from the Madeira archipelago

Received:
Revised:
Accepted:
Published online:

Abstract

The chromosomal radiation of the house mouse in the island of Madeira most likely involved a human-mediated colonization event followed by within-island geographical isolation and recurrent episodes of genetic drift. The genetic signature of such processes was assessed by an allozyme analysis of the chromosomal races from Madeira. No trace of a decrease in diversity was observed suggesting the possibility of large founder or bottleneck sizes, multiple introductions and/or a high post-colonization expansion rate. The Madeira populations were more closely related to those of Portugal than to other continental regions, in agreement with the documented human colonization of the island. Such a Portuguese origin contrasts with a study indicating a north European source of the mitochondrial haplotypes present in the Madeira mice. This apparent discrepancy may be resolved if not one but two colonization events took place, an initial north European introduction followed by a later one from Portugal. Asymmetrical reproduction between these mice would have resulted in a maternal north European signature with a nuclear Portuguese genome. The extensive chromosomal divergence of the races in Madeira is expected to contribute to their genic divergence. However, there was no significant correlation between chromosomal and allozyme distances. This low apparent chromosomal impact on genic differentiation may be related to the short time since the onset of karyotypic divergence, as the strength of the chromosomal barrier will become significant only at later stages.

  • Subscribe to Heredity for full access:

    $391

    Subscribe

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

References

  1. , (1988). The Archipelago of Madeira in the XV-Century Colecção Atlântica. Secretaria Regional do Turismo e Cultura & Centro de Estudos de História do Atlântico (eds). Região Autónoma da Madeira, Madeira, 69 pp.

  2. , (2005). Chromosome speciation: humans, Drosophila and mosquitoes. Proc Natl Acad Sci 102: 6535–6542.

  3. , , , , (1996–2004). GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR. 5171, Université de Montpellier II: Montpellier, France.

  4. , (2005). The house mouse: a model and motor for evolutionary understanding. Biol J Linn Soc 84: 335–347.

  5. (1990). Genic differentiation in M. m. domesticus populations from Europe, the Middle East and North Africa: geographic patterns and colonization events. Biol J Linn Soc 41: 27–45.

  6. , , , , , , et al. (2005). Chromosomal phylogeny of Robertsonian races of the house mouse on the island of Madeira: testing between alternative mutational processes. Genet Res 86: 171–183.

  7. , , , , , et al. (2000). Rapid chromosomal evolution in island mice. Nature 403: 158.

  8. , , , (1989). Genic differentiation and origin of Robertsonian populations of the house mouse (Mus musculus domesticus Rutty). Genet Res 53: 29–44.

  9. , , (2006). Bayesian modification of stock mixtures from molecular data. Fish Bull 104: 550–558.

  10. , (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.

  11. , , (2002). A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11: 2571–2581.

  12. (2002). Evolution on oceanic islands: molecular phylogenetic approaches to understanding pattern and process. Mol Ecol 11: 951–966.

  13. , (2005). Species diversity can drive speciation. Nature 434: 1015–1017.

  14. , , (1992). Analysis of molecular variance inferred from metric distances among haplotypes: application to human mitochondrial DNA restriction data. Genetics 31: 479–491.

  15. (1985). Phylogenies and the comparative method. Am Nat 125: 1–15.

  16. (1997). Do island populations have less genetic variation than mainland populations? Heredity 78: 311–327.

  17. , , , , , et al. (2003). The non-random occurrence of Robertsonian fusion in the house mouse. Genet Res 81: 33–42.

  18. , (2005). Dynamic patterns of adaptative radiation. Proc Natl Acad Sci 102: 18040–18045.

  19. , , , , , et al. (2001). Molecular studies on the colonization of the Madeiran archipelago by house mice. Mol Ecol 10: 2023–2029.

  20. , , , , , (1995). Differential male genetic success determines gene flow in an experimentally manipulated mouse population. Proc R Soc Lond B 260: 251–256.

  21. , (2004). The origin and radiation of Macaronesian beetles breeding in Euphorbia: the relative importance of multiple data partitions and population sampling. Syst Biol 53: 711–734.

  22. , , , (2003). Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18: 189–197.

  23. , , , , , et al. (2004). Adaptive energetics in house mice, Mus musculus L. from the island of Porto Santo (Madeira archipelago, North Atlantic). Comp Biochem Physiol A 137: 703–709.

  24. , , , , (2005). Invasion form the cold past: extensive introgression of mountain hare (Lepus timidus) mitochondrial DNA into three other hare species in northern Iberia. Mol Ecol 14: 2459–2464.

  25. , , , (1994). Mitochondrial DNA variation and the evolution of Robertsonian chromosomal races of house mice Mus domesticus. Genetics 136: 1105–1120.

  26. , (1995). Why is the house mouse karyotype so variable? Trends Ecol Evol 10: 397–402.

  27. , (1989). Genetic structure of insular Mediterranean populations of the house mouse. Biol J Linn Soc 36: 377–390.

  28. (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583–590.

  29. (2005). Bottlenecks, genetic polymorphism, and speciation. Genetics 170: 1–4.

  30. , , , , , et al. (2005). Influence of physical environmental characteristics and anthropogenic factors on the position and structure of a contact zone between chromosomal races of the house mouse on the island of Madeira (North Atlantic, Portugal). J Biogeogr 32: 2123–2134.

  31. (1996). TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12: 357–358.

  32. , (2001). Female meiosis drives karyotypic evolution in mammals. Genetics 159: 1179–1189.

  33. , , (2005). Chromosomal variation in the house mouse: a review. Biol J Linn Soc 84: 535–563.

  34. , (1995). Genepop (Version 1.2): population genetics software for exact tests and ecumenism. J Hered 86: 248–249.

  35. , (1987). Asymmetries in mating preferences between species: female swordtails prefer heterospecific males. Science 236: 595–596.

  36. , , , (2004). Mitochondrial DNA variation and population structure of the island endemic Azorean bat (Nyctalus azoreum). Mol Ecol 13: 3357–3366.

  37. (2002). Conflict between nuclear and mitochondrial DNA phylogenies of a recent species radiation: what mtDNA reveals and conceals about modes of speciation in Hawaiian crickets. Proc Natl Acad Sci 99: 16122–16127.

  38. (2004). The ghost of competition past in the phylogeny of island endemic plants. J Ecol 92: 168–173.

  39. , , (2004). Strong premating divergence in a unimodal hybrid zone between two subspecies of the house mouse. J Evol Biol 17: 165–176.

  40. , (1981). BIOSYS-1. A Computer Program for the Analysis of Allelic Variation in Population Genetics and Biochemical Systematics Release 1.7. University of Illinois: Urbana, IL.

  41. , , , , (2000). Nuclear DNA microsatellite analysis of genetic diversity and gene flow in the Scandinavian brown bear (Ursus arctos). Mol Ecol 9: 421–431.

  42. , , (2003). A rapid population expansion retains genetic diversity within European rabbits in Australia. Mol Ecol 12: 789–794.

Download references

Acknowledgements

We are extremely grateful to Claude Berger who performed part of the allozyme analysis and to Ana Isabel Galvão, Carla Cristina Marques and Ruben Capela for their help in the field. We also thank Manuel Biscoito and Jorge Prudêncio. This study was financially supported by an ICCTI–French Embassy scientific collaboration, a grant from Fundação para a Ciência e a Tecnologia (PRAXIS/PCNA/C/BIA/135/96) and funding by a SAPIENS project (POCTI/BSE/47019/02). This is publication N°ISEM2007-062.

Author information

Affiliations

  1. Institut des Sciences de l'Evolution (UM2, CNRS), Laboratoire Génétique et Environnement, CC65, Université Montpellier II, Montpellier, France

    • J Britton-Davidian
    • , J Catalan
    • , J Lopez
    • , G Ganem
    •  & J C Auffray
  2. Centro de Biologia Ambiental, Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Bloco C2, Campo Grande, Lisboa, Portugal

    • A C Nunes
    •  & M L Mathias
  3. Centro de Biologia Ambiental, Departamento Zoológico e Anthropológico do MNHN, Universidade de Lisboa, Rua da Escola Politécnica, Lisboa, Portugal

    • M G Ramalhinho
  4. Department of Biology, University of York, York, UK

    • J B Searle

Authors

  1. Search for J Britton-Davidian in:

  2. Search for J Catalan in:

  3. Search for J Lopez in:

  4. Search for G Ganem in:

  5. Search for A C Nunes in:

  6. Search for M G Ramalhinho in:

  7. Search for J C Auffray in:

  8. Search for J B Searle in:

  9. Search for M L Mathias in:

Corresponding author

Correspondence to J Britton-Davidian.

Appendices

Appendix A

The distribution of allelic frequencies at the 25 polymorphic loci in the samples studied is given in Appendix Table A1.

Table 1: Genetic diversity parameters for the 33 loci studied in the populations sampled