Data from: Genomic evidence for role of inversion 3RP of Drosophila melanogaster in facilitating climate change adaptation

Chromosomal inversion polymorphisms are common in animals and plants, and recent models suggest that alternative arrangements spread by capturing different combinations of alleles acting additively or epistatically to favour local adaptation. It is also thought that inversions typically maintain favoured combinations for a long time by suppressing recombination between alternative chromosomal arrangements. Here, we consider patterns of linkage disequilibrium and genetic divergence in an old inversion polymorphism in Drosophila melanogaster (In(3R)Payne) known to be associated with climate change adaptation and a recent invasion event into Australia. We extracted, karyotyped and sequenced whole chromosomes from two Australian populations, so that changes in the arrangement of the alleles between geographically separated tropical and temperate areas could be compared. Chromosome-wide linkage disequilibrium (LD) analysis revealed strong LD within the region spanned by In(3R)Payne. This genomic region also showed strong differentiation between the tropical and the temperate populations, but no differentiation between different karyotypes from the same population, after controlling for chromosomal arrangement. Patterns of differentiation across the chromosome arm and in gene ontologies were enhanced by the presence of the inversion. These data support the notion that inversions are strongly selected by bringing together combinations of genes, but it is still not clear if such combinations act additively or epistatically. Our data suggest that climatic adaptation through inversions can be dynamic, reflecting changes in the relative abundance of different forms of an inversion and ongoing evolution of allelic content within an inversion.

染色体倒位多态性（chromosomal inversion polymorphisms）在动物与植物中普遍存在。现有最新模型提出，不同的染色体倒位排列通过捕获不同等位基因组合（这些等位基因以加性或上位性效应促进本地适应）实现扩散；另有观点认为，倒位通常可通过抑制不同染色体倒位排列间的重组，长期维持受青睐的等位基因组合。本研究针对黑腹果蝇（Drosophila melanogaster）中一处古老的倒位多态性——In(3R)Payne——展开分析，该倒位已被证实与气候适应及近年入侵澳大利亚的事件相关。我们从两个澳大利亚种群中提取全染色体并完成核型分析与测序，以对比地理分隔的热带与温带种群间等位基因排列的差异。全染色体范围的连锁不平衡（linkage disequilibrium, LD）分析显示，In(3R)Payne覆盖的基因组区域内存在极强的连锁不平衡；该基因组区域在热带与温带种群间同样表现出显著遗传分化，但在控制染色体排列背景后，同一种群内的不同核型间并无遗传分化。倒位的存在强化了染色体臂及基因本体（gene ontologies）中的分化模式。本研究数据支持“倒位通过聚合基因组合受到强烈选择”的观点，但此类基因组合的作用方式究竟为加性还是上位性仍不明确；此外，我们的结果表明，通过倒位实现的气候适应具有动态性，其体现为倒位不同亚型的相对丰度变化，以及倒位内部等位基因内容的持续演化。