Complex genetic determinism of male-fertility restoration in the gynodioecious snail Physa acuta
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Abstract
Male fertility in plants is often controlled by the interaction between mitochondrial and nuclear genes. Some mitotypes confer cytoplasmic male sterility (CMS), making the individual male-sterile, unless the nuclear background contains alleles called restorers, that suppress the effects of CMS and restore the hermaphroditic phenotype. Restorers in cultivated crops are often alleles with strong and dominant effect, but in wild plants, data often suggest more complex systems. Here, we characterized the inheritance and specificity of restoration in a new CMS model, the freshwater snail Physa acuta . We explored two different populations (i) a naive population i.e., without contact with CMS in the past 80 generations, (ii) a non-naive population, where CMS is present and largely restored. Although we found male fertility of individuals with CMS mitogenomes to be heritable in both contexts, this genetic determinism was of a different nature depending on population history. In naive populations not coevolved with CMS the background variation may include alleles that happen to act as weak quantitative modifiers of the penetrance of CMS, while in populations coevolved with CMS, selection may have favored, when such variants were available, the emergence of strong alleles with a dominant effect.
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The study titled "Complex genetic determination of male-fertility restoration in the gynodioecious snail Physa acuta" by Skarlou et al. (doi.org/10.1101/2024.08.08.607164) investigates the genetic mechanisms underlying male fertility restoration in the freshwater snail Physa acuta, a species exhibiting gynodioecy—a reproductive system where both hermaphroditic and female individuals coexist.
In many plant species, cytoplasmic male sterility (CMS) arises from interactions between mitochondrial genes causing male sterility and nuclear genes known as restorers that can suppress this effect, restoring male fertility. While CMS is well-documented in plants, it was unknown in animals until it was recently described in Physa acuta (David et al., 2022), where it was found that different CMS factors were associated with strikingly divergent …The study titled "Complex genetic determination of male-fertility restoration in the gynodioecious snail Physa acuta" by Skarlou et al. (doi.org/10.1101/2024.08.08.607164) investigates the genetic mechanisms underlying male fertility restoration in the freshwater snail Physa acuta, a species exhibiting gynodioecy—a reproductive system where both hermaphroditic and female individuals coexist.
In many plant species, cytoplasmic male sterility (CMS) arises from interactions between mitochondrial genes causing male sterility and nuclear genes known as restorers that can suppress this effect, restoring male fertility. While CMS is well-documented in plants, it was unknown in animals until it was recently described in Physa acuta (David et al., 2022), where it was found that different CMS factors were associated with strikingly divergent mitochondrial types. This further study aims to elucidate the inheritance and specificity of male-fertility restoration in P. acuta, providing insights into CMS dynamics in animal systems.The researchers contrasted lines originating from two natural populations of P. acuta: a "naïve" population with no recent exposure to CMS and a "non-naïve" population where one CMS type is prevalent and largely restored. They found that restoration potential is heritable in both populations and specific to the CMS type. In the naïve population, certain alleles act as weak quantitative modifiers, partially restoring male fertility without prior selection pressure. In the non-naïve population, strong, dominant restorer alleles have evolved, effectively counteracting CMS due to historical selection pressures. These strong alleles were however unable to restore CMS associated with another mitochondrial type.
This study provides the first characterizations of nuclear restorers of CMS in an animal model, highlighting the complexity and variability of genetic interactions involved. It demonstrates that CMS and its restoration are not exclusive to plants and that similar genetic conflicts can shape reproductive strategies in animals. By revealing how population history influences the evolution of restorer alleles, the research offers insights into the coevolutionary dynamics between mitochondrial and nuclear genomes, advancing our understanding of sexual system evolution in hermaphroditic species.References
Elpida Skarlou, Fanny Laugier, Kévin Béthune, Timothée Chenin, Jean-Marc Donnay, Céline Froissard, Patrice David (2025) Complex genetic determinism of male-fertility restoration in the gynodioecious snail Physa acuta. bioRxiv, ver.3 peer-reviewed and recommended by PCI Evolutionary Biology https://doi.org/10.1101/2024.08.08.607164
David, P., Degletagne, C., Saclier, N., Jennan, A., Jarne, P., Plenet, S., Konecny, L., Francois, C., Gueguen, L., Garcia, N., Lefebure, T., & Luquet, E. (2022). Extreme mitochondrial DNA divergence underlies genetic conflict over sex determination. Current Biology, 32(10), 2325-2333.e6. https://doi.org/10.1016/j.cub.2022.04.014
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