Mutation load at a mimicry supergene sheds new light on the evolution of inversion polymorphisms

Type Article
Date 2021-03
Language English
Author(s) Jay PaulORCID1, Chouteau MathieuORCID1, 2, Whibley Annabel3, Bastide Héloïse4, Parrinello Hugues5, Llaurens Violaine4, Joron MathieuORCID1
Affiliation(s) 1 : CEFE, Université de Montpellier, CNRS, EPHE, IRD, Université Paul Valéry Montpellier 3, Montpellier, France
2 : LEEISA, Université de Guyane, CNRS, IFREMER, Cayenne, French Guiana
3 : School of Biological Sciences, University of Auckland, Auckland, New Zealand
4 : ISYEB, MNHN, CNRS, Sorbonne Universités, EPHE, Paris, France
5 : MGX, Biocampus Montpellier, Université de Montpellier, CNRS, INSERM, Montpellier, France
Source Nature Genetics (1061-4036) (Springer Science and Business Media LLC), 2021-03 , Vol. 53 , N. 3 , P. 288-293
DOI 10.1038/s41588-020-00771-1
WOS© Times Cited 53

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 mammals1,2,3,4,5,6,7,8,9,10,11. 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.

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