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Open Access Research article

Evolutionary dynamics of autosomal-heterosomal rearrangements in a multiple-X chromosome system of tiger beetles (Cicindelidae)

José Galián1*, Sónia JR Proença2 and Alfried P Vogler34

Author Affiliations

1 Área de Biología Animal, Departamento de Zoología y Antropología Física, Universidad de Murcia, Apdo 4021, Murcia 30071, Spain

2 Centro de Biologia Ambiental/Departamento de Zoologia e Antropologia, Faculdade de Ciências, Universidade de Lisboa, Campo Grande, Bloco C2 – 3° Piso, 1700 Lisboa, Portugal

3 Department of Entomology, Natural History Museum, London, SW7 5BD, UK

4 Department of Biology, Imperial College London, Silwood Park Campus, Ascot, Berkshire, SL5 7PY, UK

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BMC Evolutionary Biology 2007, 7:158  doi:10.1186/1471-2148-7-158

Published: 6 September 2007

Abstract

Background

Genetic systems involving multiple X chromosomes have arisen repeatedly in sexually reproducing animals. Tiger beetles (Cicindelidae) exhibit a phylogenetically ancient multiple-X system typically consisting of 2–4 X chromosomes and a single Y. Because recombination rates are suppressed in sex chromosomes, changes in their numbers and movement of genes between sex chromosomes and autosomes, could have important consequences for gene evolution and rates of speciation induced by these rearrangements. However, it remains unclear how frequent these rearrangements are and which genes are affected.

Results

Karyotype analyses were performed for a total of 26 North American species in the highly diverse genus Cicindela, tallying the number of X chromosomes and autosomes during mitosis and meiosis. The chromosomal location of the ribosomal rRNA gene cluster (rDNA) was used as an easily scored marker for genic turnover between sex chromosomes or autosomes. The findings were assessed in the light of a recent phylogenetic analysis of the group. While autosome numbers remained constant throughout the lineage, sex chromosome numbers varied. The predominant karyotype was n = 9+X1X2X3Y which was also inferred to be the ancestral state, with several changes to X1X2Y and X1X2X3X4Y confined to phylogenetically isolated species. The total (haploid) numbers of rDNA clusters varied between two, three, and six (in one exceptional case), and clusters were localized either on the autosomes, the sex chromosomes, or both. Transitions in rDNA localization and in numbers of rDNA clusters varied independently of each other, and also independently of changes in sex chromosome numbers.

Conclusion

Changes of X chromosome numbers and transposition of the rDNA locus (and presumably other genes) between autosomes and sex chromosomes in Cicindela occur frequently, and are likely to be the result of fusions or fissions between X chromosomes, rather than between sex chromosomes and autosomes. Yet, translocations between sex chromosomes and autosomes appear to be common, as indicated by the patterns of rDNA localization. Rearranged karyotypes involving multiple sex chromosomes would reduce recombination, and hybrid dysgenesis selects against polymorphic populations. Hence, the high frequency of these rearrangements could be a cause of the great species diversity in Cicindela.