The Evolutionary Dynamics of Cytoplasmic Male Sterility

Abstract

Cytoplasmic male sterility (CMS) is the maternal transmission of failed pollen production in hermaphroditic plants leading to a mixture of male-sterile and hermaphroditic individuals in the population (gynodioecy). Autosomal genes that can restore pollen fertility in the presence of male-sterile cytotypes are commonly observed. CMS in wild populations tends to be associated with (1) the maintenance of distinct cytotypes, each capable of causing male sterility by an apparently different mechanism since each is susceptible to only a particular subset of autosomal restorer alleles; (2) the maintenance of polymorphism at several autosomal restorer loci, with particular alleles or loci specialized for restoring pollen fertility when associated with particular cytotypes; (3) the maintenance of genetic differentiation among geographically distant populations; and (4) the maintenance of phenotypic diversity among populations, measured as the percentage of malesterile individuals. Observations and previous theoretical explanations were reviewed. A simulation model was then constructed, and the results of the simulations appear to be consistent with the evolutionary dynamics and patterns of genetic polymorphism inferred from wild populations. In the simulation models, when cytoplasmic male-sterility alleles are present and their associated autosomal pollen-restorer alleles are absent (cytoplasmic control), the frequency of females increases because of the ovule-fitness advantage usually associated with male sterility. When autosomal restorer alleles are present (autosomal control), the frequency of females tends to decline. The opposite directions of evolution favored by the cytoplasm and autosomes reflect the inherent conflict of interest between genomic subsets over the sex-allocation ratio. The evolutionary dynamics depend on an interaction between the phenotypic and genotypic frequencies and on the continual loss and reintroduction of genetic novelty over evolutionary time. A striking difference was observed between the potential genetic control of male sterility built into the simulation model, which reflects assumptions about the underlying physiological mechanisms of normal and aberrant pollen production, and the types of genetic control that would be inferred by performing classical genetic crossing experiments on a sample of the simulated population. This contrast between potential and inferred control is possibly an important general attribute of traits that are the resolution of a continual evolutionary conflict.