Abstract
BackgroundGenetic 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.ResultsKaryotype 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.ConclusionChanges 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.
Highlights
Genetic systems involving multiple X chromosomes have arisen repeatedly in sexually reproducing animals
We found the X1X2X3Y genetic system in several species which in the older literature were reported to exhibit a single X chromosome
Our analysis found four species each showing X1X2X3X4Y (C. lemniscata, C. marutha, C. nigrocoerulea and C. marginata) or X1X2Y (C. sedecimpunctata, C. ocellata, C. rugatilis, C. nebuligera) (Table 1)
Summary
Genetic systems involving multiple X chromosomes have arisen repeatedly in sexually reproducing animals. 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. It remains unclear how frequent these rearrangements are and which genes are affected. As rearrangements would change the position of genes, generating new linkage groups that may lead to an increase of genetic differentiation between populations, they are expected to restrict reproductive compatibility and eventually promote speciation. As the result of reduced recombination, genetic barriers to gene flow may arise rapidly between populations which are fixed for sex chromosomal variants
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