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Extreme mitochondrial DNA divergence underlies genetic conflict over sex determination

Abstract : Cytoplasmic male-sterility (CMS) is a form of genetic conflict over sex determination that results from differences in modes of inheritance between genomic compartments 1-3. Indeed, maternally-transmitted (usually mitochondrial) genes, sometimes enhance their transmission by suppressing the male function in a hermaphroditic organism, to the detriment of biparentallyinherited nuclear genes. As a result, these hermaphrodites become functionally female, and may coexist with regular hermaphrodites in so-called gynodioecious populations 3. CMS has been known in plants since Darwin's times 4 , but is previously unknown in the animal kingdom 5-8. We relate the first observation of CMS in animals. It occurs in a freshwater snail population, where some individuals appear unable to sire offspring in controlled crosses and show anatomical, physiological and behavioral characters consistent with a suppression of the male function. Male-sterility is associated with a mitochondrial lineage that underwent a spectacular acceleration of DNA substitution rates, affecting the entire mitochondrial genome-this acceleration concerns both synonymous and nonsynonymous substitutions and therefore results from increased mitogenome mutation rates. Consequently, mitochondrial haplotype divergence within the population is exceptionally high, matching that observed between snail taxa that diverged 475 million years ago. This result is reminiscent of similar accelerations in mitogenome evolution observed in plant clades where gynodioecy is frequent 9,10 , both being consistent with arms-race evolution of genome regions implicated in CMS 11,12. Our study shows that genomic conflicts can trigger independent evolution of similar sex determination systems in plants and animals, and dramatically accelerate molecular evolution.
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Submitted on : Wednesday, August 31, 2022 - 3:20:56 PM
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Patrice David, Cyril Degletagne, Nathanaelle Saclier, Aurel Jennan, Philippe Jarne, et al.. Extreme mitochondrial DNA divergence underlies genetic conflict over sex determination. Current Biology - CB, Elsevier, 2022, 32 (10), pp.2325-2333.e6. ⟨10.1016/j.cub.2022.04.014⟩. ⟨hal-03765839⟩

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