Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland.
Department of Biology, University of Fribourg, Fribourg, Switzerland.
Mol Biol Evol. 2023 Jun 1;40(6). doi: 10.1093/molbev/msad118.
Since the pioneering work of Dobzhansky in the 1930s and 1940s, many chromosomal inversions have been identified, but how they contribute to adaptation remains poorly understood. In Drosophila melanogaster, the widespread inversion polymorphism In(3R)Payne underpins latitudinal clines in fitness traits on multiple continents. Here, we use single-individual whole-genome sequencing, transcriptomics, and published sequencing data to study the population genomics of this inversion on four continents: in its ancestral African range and in derived populations in Europe, North America, and Australia. Our results confirm that this inversion originated in sub-Saharan Africa and subsequently became cosmopolitan; we observe marked monophyletic divergence of inverted and noninverted karyotypes, with some substructure among inverted chromosomes between continents. Despite divergent evolution of this inversion since its out-of-Africa migration, derived non-African populations exhibit similar patterns of long-range linkage disequilibrium between the inversion breakpoints and major peaks of divergence in its center, consistent with balancing selection and suggesting that the inversion harbors alleles that are maintained by selection on several continents. Using RNA-sequencing, we identify overlap between inversion-linked single-nucleotide polymorphisms and loci that are differentially expressed between inverted and noninverted chromosomes. Expression levels are higher for inverted chromosomes at low temperature, suggesting loss of buffering or compensatory plasticity and consistent with higher inversion frequency in warm climates. Our results suggest that this ancestrally tropical balanced polymorphism spread around the world and became latitudinally assorted along similar but independent climatic gradients, always being frequent in subtropical/tropical areas but rare or absent in temperate climates.
自 20 世纪 30 年代和 40 年代 Dobzhansky 的开创性工作以来，已经鉴定出许多染色体倒位，但它们如何促进适应仍然知之甚少。在黑腹果蝇中，广泛存在的倒位多态性 In(3R)Payne 支撑着多个大陆上适应度特征的纬度梯度。在这里，我们使用个体全基因组测序、转录组学和已发表的测序数据研究了这个在四个大陆上的种群基因组学：在其祖先的非洲范围内和在欧洲、北美和澳大利亚的衍生种群中。我们的结果证实，这个倒位起源于撒哈拉以南非洲，随后变得世界性；我们观察到倒位和非倒位染色体的明显单系分化，在大陆之间的倒位染色体之间存在一些亚结构。尽管这个倒位自走出非洲以来发生了分歧进化，但衍生的非非洲种群表现出与倒位断点和中心主要分化峰之间的长程连锁不平衡相似的模式，这与平衡选择一致，并表明这个倒位携带由几个大陆上的选择维持的等位基因。使用 RNA-seq，我们鉴定了与倒位相关的单核苷酸多态性和在倒位和非倒位染色体之间差异表达的基因座之间的重叠。在低温下，倒位染色体的表达水平更高，这表明缓冲或补偿性可塑性的丧失，与温暖气候中更高的倒位频率一致。我们的结果表明，这个起源于热带的平衡多态性在世界各地传播，并沿着类似但独立的气候梯度进行纬度分类，在亚热带/热带地区总是频繁，但在温带地区很少或不存在。
