Chromosomal inversion polymorphisms and adaptation

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Chromosomal inversion polymorphisms continue to be identified from an increasing number of populations of insects, plants, bacteria and humans. In the fruit fly Drosophila, chromosomal polymorphisms were used in classic studies of natural selection. Recent molecular genetic studies suggest that inversion polymorphisms are dynamical systems. These studies also indicate patterns of disequilibrium and variation that are consistent with co-adapted gene complexes. Although these complexes have yet to be identified, recent studies have identified traits, such as body size, that are linked to inversion polymorphisms. Selection acting on these polymorphisms is strong because latitudinal clines in inversion frequency become re-established rapidly after a new continent is colonized. A combined molecular and phenotypic approach is helping to identify the role of inversion polymorphisms in adaptive divergence, but the genes responsible for associations between traits and inversion polymorphisms remain to be identified.

Section snippets

Distribution of inversion polymorphisms

Inversion polymorphisms usually involve paracentric rather than pericentric inversions [4]. Paracentric polymorphisms are common in dipterans other than Drosophila, including midges 5, 6 and mosquitoes; in the species complex of Anopheles gambiae mosquitoes, >120 polymorphic inversions occur in natural populations [7]. Paracentric inversions have probably resulted from the homologous recombination of repetitive elements such as transposons because transposable elements have been found at

Changes in inversion frequencies

Clinal variation in traits and genetic variants along latitudinal or altitudinal gradients provides strong evidence for the effects of natural selection associated with climatic factors. Stable latitudinal clines for inversion frequencies in Drosophila are repeatable across continents and are often associated with climatic variables (reviewed in [4]). These clines suggest that there are likely to be beneficial effects associated with inversions. Inversion frequencies in Anopheles mosquitoes,

Inversions, traits and fitness

Which traits are associated with inversion polymorphisms, and why is variation in only some traits tied to inversions? In Drosophila, traits that have been linked to inversion polymorphisms include viability, development time, longevity, mating success, fecundity, bristle number, resistance to thermal extremes and body size (Table 1). In mosquitoes, inversions have also been linked to some of these traits, as well as resistance to DDT and dieldrin pesticides [25]. In chironomids, inversion

Patterns of variation within inversions

Given that inversions inhibit recombination with standard arrangements, loci within newly arisen monophyletic inversions will be in strong linkage disequilibrium. However, rare multiple crossovers within the breakpoints of an inversion will produce viable gametes and, therefore, genetic exchange (or recombination) can occur between standard and inverted chromosomes. In addition, gene conversion will still operate in an unrestricted fashion in inversion heterozygotes [51], except perhaps around

Concluding remarks

Molecular studies of inversions have confirmed previous views that inversions are associated with disequilibrium among loci, suggesting that they have the potential to lock up co-adapted alleles. Progress has been made in identifying traits associated with inversions and the different processes that might be involved in maintaining inversion polymorphisms in populations. A challenge is to identify the specific genes involved and why these are locked within inversions. There are several

Acknowledgements

We thank the Australian Research Council for financial support via their Special Research Centre Program, Alisha Anderson for the photograph of In(3R)Payne, and three anonymous reviewers for constructive criticisms.

Glossary

Fitness epistasis:
interactions between alleles (genes) that affect fitness.
Frequency-dependent selection:
the fitness of a genotype (or chromosome arrangement) is dependent on the relative frequency of other genotypes (arrangements) in a population.
Gene conversion:
a nonreciprocal transfer of genetic information during recombination.
Heterosis (for inversion polymorphisms):
individuals that are heterozygous for an inversion arrangement exhibit a higher relative fitness than do individuals that are

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