Department of Entomology, Virginia Tech, Blacksburg, VA 24061, USA.
BMC Evol Biol. 2011 Apr 7;11:91. doi: 10.1186/1471-2148-11-91.
The malaria mosquito species of subgenus Cellia have rich inversion polymorphisms that correlate with environmental variables. Polymorphic inversions tend to cluster on the chromosomal arms 2R and 2L but not on X, 3R and 3L in Anopheles gambiae and homologous arms in other species. However, it is unknown whether polymorphic inversions on homologous chromosomal arms of distantly related species from subgenus Cellia nonrandomly share similar sets of genes. It is also unclear if the evolutionary breakage of inversion-poor chromosomal arms is under constraints.
To gain a better understanding of the arm-specific differences in the rates of genome rearrangements, we compared gene orders and established syntenic relationships among Anopheles gambiae, Anopheles funestus, and Anopheles stephensi. We provided evidence that polymorphic inversions on the 2R arms in these three species nonrandomly captured similar sets of genes. This nonrandom distribution of genes was not only a result of preservation of ancestral gene order but also an outcome of extensive reshuffling of gene orders that created new combinations of homologous genes within independently originated polymorphic inversions. The statistical analysis of distribution of conserved gene orders demonstrated that the autosomal arms differ in their tolerance to generating evolutionary breakpoints. The fastest evolving 2R autosomal arm was enriched with gene blocks conserved between only a pair of species. In contrast, all identified syntenic blocks were preserved on the slowly evolving 3R arm of An. gambiae and on the homologous arms of An. funestus and An. stephensi.
Our results suggest that natural selection favors specific gene combinations within polymorphic inversions when distant species are exposed to similar environmental pressures. This knowledge could be useful for the discovery of genes responsible for an association of inversion polymorphisms with phenotypic variations in multiple species. Our data support the chromosomal arm specificity in rates of gene order disruption during mosquito evolution. We conclude that the distribution of breakpoint regions is evolutionary conserved on slowly evolving arms and tends to be lineage-specific on rapidly evolving arms.
细胞亚属疟蚊种具有丰富的与环境变量相关的倒位多态性。在冈比亚按蚊和其他物种的同源臂中，多态倒位往往聚集在 2R 和 2L 染色体臂上，但不在 X、3R 和 3L 上。然而，目前尚不清楚细胞亚属远缘物种的同源染色体臂上的多态倒位是否随机共享相似的基因集。也不清楚缺乏倒位的染色体臂的进化断裂是否受到限制。
为了更好地理解臂特异性基因组重排率的差异，我们比较了基因顺序，并在冈比亚按蚊、致倦库蚊和斯蒂芬斯按蚊之间建立了同线性关系。我们提供的证据表明，这三个物种的 2R 臂上的多态倒位随机捕获了相似的基因集。这种基因的非随机分布不仅是祖先基因顺序保存的结果，也是基因顺序广泛重排的结果，这种重排在独立起源的多态倒位中创造了同源基因的新组合。保守基因顺序分布的统计分析表明，常染色体臂在产生进化断点方面存在差异。进化最快的 2R 常染色体臂富含仅在一对物种之间保守的基因块。相比之下，在冈比亚按蚊的缓慢进化的 3R 臂和致倦库蚊和斯蒂芬斯按蚊的同源臂上都保留了所有鉴定的同线性块。
我们的结果表明，当远缘物种受到相似的环境压力时，自然选择有利于多态倒位中的特定基因组合。当涉及到多个物种的与倒位多态性相关的表型变异的基因时，这些知识可能是有用的。我们的数据支持蚊类进化过程中基因顺序破坏的染色体臂特异性。我们得出结论，在缓慢进化的臂上，断点区域的分布在进化上是保守的，而在快速进化的臂上则倾向于具有谱系特异性。
