Paternal Cytoplasmic Inheritance

We continue our study of the effects of pollen and seed migration on the cytonuclear structure of mixed-mating plant populations by analyzing two deterministic continent-island models under the critical assumption of paternal cytoplasmic inheritance. The major results of this study that contrast with our previous conclusions based on maternal cytoplasmic inheritance are (i) pollen gene flow can significantly affect the cytonuclear structure of the island population, and in particular can help to generate cytonuclear disequilibria that greatly exceed the magnitude of those that would be produced by seed migration or mixed mating alone; (ii) with simultaneous pollen and seed migration, nonzero cytonuclear disequilibria will be maintained not only when there is disequilibrium in the immigrant pollen or seeds, but also through a variety of intermigrant admixture effects when the two pools of immigrants differ appropriately in their cytonuclear compositions; (iii) either immigrant pollen or immigrant seeds can generate disequilibria de novo in populations with initially random cytonuclear associations, but pollen migration alone generally produces lower levels of disequilibrium than does comparable seed migration, especially at high levels of self-fertilization when the overall fraction of immigrant pollen is low; (iv) the equilibrium state of the island population will be influenced by the rate of pollen gene flow whenever there is either allelic disequilibrium in the immigrant pollen or simultaneous seed migration coupled with different cytoplasmic or nuclear allele frequencies in immigrant pollen and seeds or nonzero allelic disequilibrium in either immigrant pool. The estimation of pollen migration should therefore be facilitated with paternal cytoplasmic inheritance relative to the case of maternal cytoplasmic inheritance. These basic conclusions hold whether the population is censused as seeds or as adults, but with simultaneous pollen and seed migration, the relationship between census time and the ability to detect nonrandom cytonuclear associations is complex. When migration is through pollen alone, however, the cytonuclear structure of the island population is independent of the life stage censused. T HE consideration of joint nuclear and cytoplasmic polymorphisms provides a novel approach to the study of migration in natural populations. For example, gene flow models incorporating a single nuclear locus and a uniparentally inherited, cytoplasmic locus have been used to investigate mitochondrial gene flow between Drosophila species (TAKAHATA and SLATKIN 1984) and rates of migration from parental species into hybrid zones of frogs and eels (ASMUSSEN, ARNOLD and AVISE 1989; AVISE et al. 1990). Theoretical studies also have shown how cytonuclear frequencies, and especially the nonrandom associations (disequilibria) between the corresponding single-locus frequencies, can identify zones of admixture and can provide estimates of gene flow between one or more random-mating populations (ASMUSSEN and ARNOLD 1991). The use of cytonuclear data might likewise enhance the study of gene flow in seed plants, which in comI Present address: University of Georgia, Savannah River Ecology Laboratory, Drawer E, Aiken, South Carolina 29802. Genetics 132: 253-267 (September, 1992) pletely and partially outcrossing species can occur through pollen and seeds. In the first paper of this series, we analyzed a set of continent-island models to delimit the effects of pollen and seed migration on cytonuclear frequencies and disequilibria in randommating, mixed-mating, and self-fertilizing populations, in which the cytoplasmic DNA was inherited maternally (ASMUSSEN and SCHNABEL 1991). In this case, pollen carries no cytoplasmic genes and seed migration accordingly has the predominant, and pollen migration only a minor, influence on the cytonuclear structure of the plant population. Although organellar DNA in plants is most commonly maternally inherited, several taxa with paternal inheritance have now been discovered. For example, based on data from several species in three families, chloroplast (cp) DNA appears to be inherited paternally in coniferous gymnosperms (WAGNER et al. 1991). More surprising, however, are studies showing paternal inheritance of mitochondrial DNA in the conifer species Sequoia semperuirens (NEALE, MARSHALL and SEDEROFF 1989) and Calocedrus decurrens 254 A. Schnabel and M. A. Asmussen