Abstract
BackgroundChromosomal inversions are increasingly being recognized as important in adaptive shifts and are expected to influence patterns of genetic variation, but few studies have examined genetic patterns in inversion polymorphisms across and within populations. Here, we examine genetic variation at 20 microsatellite loci and the alcohol dehydrogenase gene (Adh) located within and near the In(2L)t inversion of Drosophila melanogaster at three different sites along a latitudinal cline on the east coast of Australia.ResultsWe found significant genetic differentiation between the standard and inverted chromosomal arrangements at each site as well as significant, but smaller differences among sites in the same arrangement. Genetic differentiation between pairs of sites was higher for inverted chromosomes than standard chromosomes, while inverted chromosomes had lower levels of genetic variation even well away from inversion breakpoints. Bayesian clustering analysis provided evidence of genetic exchange between chromosomal arrangements at each site.ConclusionsThe strong differentiation between arrangements and reduced variation in the inverted chromosomes are likely to reflect ongoing selection at multiple loci within the inverted region. They may also reflect lower effective population sizes of In(2L)t chromosomes and colonization of Australia, although there was no consistent evidence of a recent bottleneck and simulations suggest that differences between arrangements would not persist unless rates of gene exchange between them were low. Genetic patterns therefore support the notion of selection and linkage disequilibrium contributing to inversion polymorphisms, although more work is needed to determine whether there are spatially varying targets of selection within this inversion. They also support the idea that the allelic content within an inversion can vary between geographic locations.
Highlights
Chromosomal inversions are increasingly being recognized as important in adaptive shifts and are expected to influence patterns of genetic variation, but few studies have examined genetic patterns in inversion polymorphisms across and within populations
Frequencies of the AdhS allele ranged from 0.34 to 0.91 and In(2L)t from 0.04 to 0.29. These frequencies were very close to those reported by Umina et al [28], suggesting the crossing scheme did not favour a particular alcohol dehydrogenase gene (Adh) allele or chromosome arrangement (Figure 2)
Consistent with this, our data show there is strong differentiation between chromosome arrangements at all sites, for some chromosomal regions. They show significant differentiation among In(2L)t chromosomes sampled from different sites along a latitudinal cline that is significantly greater than levels of differentiation observed at the same markers in standard chromosomes
Summary
Chromosomal inversions are increasingly being recognized as important in adaptive shifts and are expected to influence patterns of genetic variation, but few studies have examined genetic patterns in inversion polymorphisms across and within populations. We examine genetic variation at 20 microsatellite loci and the alcohol dehydrogenase gene (Adh) located within and near the In(2L)t inversion of Drosophila melanogaster at three different sites along a latitudinal cline on the east coast of Australia. In Drosophila and other Diptera, inverted and noninverted (standard) forms of chromosomes often coexist within the same population. These inversion polymorphisms numbers of species including plants [5], seaweed flies [6], butterflies [7], Anopheles mosquitoes [8], fruit flies [9] and humans [10]. Inversions maintain associations between alleles because crossing over between inverted and standard arrangements gives rise to nonfunctional meiotic products. Heterosis and the idea that the allelic content of the inversion evolves after inversions arise are assumed, leading to different alleles in populations within the same inversion [12,13]
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