Both nuclear and cytoplasmic polymorphisms are involved in genetic conflicts over male fertility in the gynodioecious snail Physa acuta

Abstract

Gynodioecy, the coexistence of hermaphrodites with females, often reflects conflicts between cytoplasmic male sterility (CMS) genes and nuclear genes restoring male fertility. CMS is frequent in plants, and has been recently discovered in one animal: the freshwater snail Physa acuta. In this system, CMS was linked to a single divergent mitochondrial genome (D), devoid of apparent nuclear restoration. Our study uncovers a second, novel CMS-associated mitogenome (K) in Physa acuta, demonstrating an extraordinary acceleration of molecular evolution throughout the entire K mitochondrial genome, akin to the previously observed pattern in D. This suggests a pervasive occurrence of accelerated evolution in both CMS-associated lineages. Through a 17-generation introgression experiment, we further show that nuclear polymorphisms in K-mitogenome individuals contribute to the restoration of male function in natural populations. Our results underscore shared characteristics in gynodioecy between plants and animals, emphasizing the presence of multiple CMS mitotypes and cyto-nuclear conflicts. This reaffirms the pivotal role of mitochondria in influencing male function and in generating genomic conflicts that impact reproductive processes in animals.

Keywords: Physa acuta; arms-race; cytoplasmic male sterility; gynodioecy; mitochondrial genomes; restoration.