CEFE, Université de Montpellier, CNRS, EPHE, IRD, Université Paul Valéry Montpellier 3, Montpellier, France.
LEEISA, Université de Guyane, CNRS, IFREMER, Cayenne, French Guiana.
Nat Genet. 2021 Mar;53(3):288-293. doi: 10.1038/s41588-020-00771-1. Epub 2021 Jan 25.
Chromosomal inversions are ubiquitous in genomes and often coordinate complex phenotypes, such as the covariation of behavior and morphology in many birds, fishes, insects or mammals. However, why and how inversions become associated with polymorphic traits remains obscure. Here we show that despite a strong selective advantage when they form, inversions accumulate recessive deleterious mutations that generate frequency-dependent selection and promote their maintenance at intermediate frequency. Combining genomics and in vivo fitness analyses in a model butterfly for wing-pattern polymorphism, Heliconius numata, we reveal that three ecologically advantageous inversions have built up a heavy mutational load from the sequential accumulation of deleterious mutations and transposable elements. Inversions associate with sharply reduced viability when homozygous, which prevents them from replacing ancestral chromosome arrangements. Our results suggest that other complex polymorphisms, rather than representing adaptations to competing ecological optima, could evolve because chromosomal rearrangements are intrinsically prone to carrying recessive harmful mutations.
染色体倒位在基因组中普遍存在,通常协调复杂的表型,如许多鸟类、鱼类、昆虫或哺乳动物的行为和形态的共变。然而,为什么倒位与多态性特征相关,以及如何相关仍然不清楚。在这里,我们表明,尽管倒位形成时具有很强的选择优势,但它们会积累隐性有害突变,从而产生频率依赖选择,并促进它们在中间频率下的维持。我们结合基因组学和体内适合度分析,以蝴蝶翅膀图案多态性的模式生物——Heliconius numata 为模型,揭示了三个具有生态优势的倒位通过有害突变和转座元件的连续积累而积累了大量的突变负荷。当纯合子时,倒位与明显降低的生存力相关联,这阻止了它们取代祖先的染色体排列。我们的研究结果表明,其他复杂的多态性,而不是代表对竞争生态最优的适应,可能是由于染色体重排本身容易携带隐性有害突变而进化的。