Abstract
BackgroundNonrandom distribution of rearrangements is a common feature of eukaryotic chromosomes that is not well understood in terms of genome organization and evolution. In the major African malaria vector Anopheles gambiae, polymorphic inversions are highly nonuniformly distributed among five chromosomal arms and are associated with epidemiologically important adaptations. However, it is not clear whether the genomic content of the chromosomal arms is associated with inversion polymorphism and fixation rates.Methodology/Principal FindingsTo better understand the evolutionary dynamics of chromosomal inversions, we created a physical map for an Asian malaria mosquito, Anopheles stephensi, and compared it with the genome of An. gambiae. We also developed and deployed novel Bayesian statistical models to analyze genome landscapes in individual chromosomal arms An. gambiae. Here, we demonstrate that, despite the paucity of inversion polymorphisms on the X chromosome, this chromosome has the fastest rate of inversion fixation and the highest density of transposable elements, simple DNA repeats, and GC content. The highly polymorphic and rapidly evolving autosomal 2R arm had overrepresentation of genes involved in cellular response to stress supporting the role of natural selection in maintaining adaptive polymorphic inversions. In addition, the 2R arm had the highest density of regions involved in segmental duplications that clustered in the breakpoint-rich zone of the arm. In contrast, the slower evolving 2L, 3R, and 3L, arms were enriched with matrix-attachment regions that potentially contribute to chromosome stability in the cell nucleus.Conclusions/SignificanceThese results highlight fundamental differences in evolutionary dynamics of the sex chromosome and autosomes and revealed the strong association between characteristics of the genome landscape and rates of chromosomal evolution. We conclude that a unique combination of various classes of genes and repetitive DNA in each arm, rather than a single type of repetitive element, is likely responsible for arm-specific rates of rearrangements.
Highlights
A growing number of studies demonstrate that chromosomal inversions facilitate genetic differentiation during speciation [1,2]
We demonstrated that the sex chromosome has the highest rate of inversion fixation, which is in contrast with the absence of polymorphic inversions on the X chromosome in the studied species (Figure 2, S3)
The X chromosome had the highest densities of transposable element (TE), microsatellites, minisatellites, and satellites, which are known for their roles in the origin of inversions [38,39,40]
Summary
A growing number of studies demonstrate that chromosomal inversions facilitate genetic differentiation during speciation [1,2]. Previous studies of chromosomal evolution using physical maps of distant Anopheles species, An. albimanus, An. gambiae, and An. funestus have demonstrated that paracentric inversions and whole-arm translocations are the major types of rearrangements and that the 2R arm has the fastest rate of inversion fixation among autosomes [12,13]. In the major African malaria vector Anopheles gambiae, polymorphic inversions are highly nonuniformly distributed among five chromosomal arms and are associated with epidemiologically important adaptations. It is not clear whether the genomic content of the chromosomal arms is associated with inversion polymorphism and fixation rates
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