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ABSTRACT: Self-incompatibility (SI) in flowering plants entails the inhibition of fertilization by pollen that express specificities in common with the pistil. In species of the Solanaceae, Rosaceae, and Scrophulariaceae, the inhibiting factor is an extracellular ribonuclease (S-RNase) secreted by stylar tissue. A distinct but as yet unknown gene (provisionally called pollen-S) appears to determine the specific S-RNase from which a pollen tube accepts inhibition. The S-RNase gene and pollen-S segregate with the classically defined S-locus. The origin of a new specificity appears to require, at minimum, mutations in both genes. We explore the conditions under which new specificities may arise from an intermediate state of loss of self-recognition. Our evolutionary analysis of mutations that affect either pistil or pollen specificity indicates that natural selection favors mutations in pollen-S that reduce the set of pistils from which the pollen accepts inhibition and disfavors mutations in the S-RNase gene that cause the nonreciprocal acceptance of pollen specificities. We describe the range of parameters (rate of receipt of self-pollen and relative viability of inbred offspring) that permits the generation of a succession of new specificities. This evolutionary pathway begins with the partial breakdown of SI upon the appearance of a mutation in pollen-S that frees pollen from inhibition by any S-RNase presently in the population and ends with the restoration of SI by a mutation in the S-RNase gene that enables pistils to reject the new pollen type.
Genetics 05/2001; 157(4):1805-17. · 4.01 Impact Factor
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M K Uyenoyama
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ABSTRACT: Many hermaphroditic plants avoid self-fertilization by rejecting pollen that express genetically-determined specificities in common with the pistil. Self-incompatibility systems typically show extremely high genetic diversity, some maintaining hundreds of specificities. This article addresses the genetic and evolutionary mechanisms through which new mating specificities arise. Recent investigations of the genetic and physiological basis of self-incompatibility are reviewed. Two evolutionary pathways are considered: one which requires full expression of self-incompatibility in all intermediates and one in which new mating specificities arise through episodes of partial breakdown and restoration of self-incompatibility.
Genes & Genetic Systems 01/2001; 75(6):305-11. · 0.95 Impact Factor
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M K Uyenoyama
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ABSTRACT: Self-incompatibility in Brassica entails the rejection of pollen grains that express specificities held in common with the seed parent. In Brassica, pollen specificity is encoded at the multipartite S-locus, a complex region comprising many expressed genes. A number of species within the Brassicaceae express sporophytic self-incompatibility, under which individual pollen grains bear specificities determined by one or both S-haplotypes of the pollen parent. Classical genetic and nucleotide-level analyses of the S-locus have revealed a dichotomy in sequence and function among S-haplotypes; in particular, all class I haplotypes show dominance over all class II haplotypes in determination of pollen specificity. Analysis of an evolutionary model that explicitly incorporates features of the Brassica system, including the class dichotomy, indicates that class II haplotypes may invade populations at lower rates and decline to extinction at higher rates than class I haplotypes. This analysis suggests convergence to an evolutionarily persistent state characterized by the maintenance in high frequency of a single class II haplotype together with many class I haplotypes, each in low frequency. This expectation appears to be consistent with empirical observations of high frequencies of relatively few distinct recessive haplotypes.
Genetics 10/2000; 156(1):351-9. · 4.01 Impact Factor
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The Plant Cell 04/2000; 12(3):310-2; author reply 313-5. · 8.99 Impact Factor
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M K Uyenoyama
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ABSTRACT: A method is proposed for characterizing the structure of genealogies among alleles that regulate self-incompatibility in flowering plants. Expected distributions of ratios of divergence times among alleles, scaled by functions of allele number, were generated by numerical simulation. These distributions appeared relatively insensitive to the particular parameter values assigned in the simulations over a fourfold range in effective population size and a 100-fold range in mutation rate. Generalized least-squares estimates of the scaled indices were obtained from genealogies reconstructed from nucleotide sequences of self-incompatibility alleles from natural populations of two solanaceous species. Comparison of the observed indices to the expected distributions generated by numerical simulation indicated that the allelic genealogy of one species appeared consistent with the symmetric balancing selection generated by self-incompatibility. However, the allelic genealogy of the second species showed unusually long terminal branches, suggesting the operation of additional evolutionary processes.
Genetics 12/1997; 147(3):1389-400. · 4.01 Impact Factor
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ABSTRACT: The self-incompatibility (S) locus of flowering plants offers an example of extreme polymorphism maintained by balancing selection. Estimates of recent and long-term effective population size (Ne) were determined for two solanaceous species by examination of S-allele diversity. Estimates of recent Ne in two solanaceous species differed by an order of magnitude, consistent with differences in the species' ecology. In one species, the evidence was consistent with historical population restriction despite a large recent Ne. In the other, no severe bottleneck was indicated over millions of years. Bottlenecks are integral to founder-event speciation, and loci that are subject to balancing selection can be used to evaluate the frequency of this mode of speciation.
Science 09/1996; 273(5279):1212-6. · 31.20 Impact Factor
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ABSTRACT: Allelic diversity at the self-incompatibility (S-) locus in the ground cherry, Physalis crassifolia (Solanaceae), was surveyed in a natural population occurring in Deep Canyon, CA, using a molecular assay to determine the genotype of individual plants. A total of 28 different S-alleles were identified and sequenced from a sample of 22 plants. All plants examined were heterozygous, as expected under gametophytic self-incompatibility (GSI). The estimated number of alleles in this population is 43-44, comparable to allelic diversity reported for other species, as determined by the standard diallel crossing method. Allele frequencies in the sample deviated from the expectation of equal frequency under GSI; it is suggested that this deviation may result from sampling of related individuals. Molecular analysis of genotypes within single pollen donor families indicates that, for all alleles examined, segregation is consistent with predictions for single-locus GSI. The implications of a reliable and efficient molecular assay for determining the S-genotype of plants are discussed.
Heredity 06/1996; 76 ( Pt 5):497-505. · 4.60 Impact Factor
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ABSTRACT: S-allele diversity in Solanum carolinense was surveyed in two natural populations, located in Tennessee and North Carolina, with a molecular assay to determine the genotype of individual plants. A total of 13 different S-alleles were identified and sequenced. There is high overlap between the two populations sampled, with 10 alleles shared in common, one allele found only in Tennessee, and two found only in North Carolina. The number of alleles in this species appears to be extremely low compared with other species with gametophytic self-incompatibility. Sequence comparisons show that most alleles are extremely different one from another in their primary sequence and a phylogenetic analysis indicates extensive trans-specific evolution of S-lineages. In addition, some alleles appear to be derived much more recently. The implications of these observations are discussed in the light of recent theoretical results on S-allele population diversity and persistence.
Heredity 11/1995; 75 ( Pt 4):405-15. · 4.60 Impact Factor
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M K Uyenoyama
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ABSTRACT: Analysis of nucleotide sequences that regulate the expression of self-incompatibility in flowering plants affords a direct means of examining classical hypotheses for the origin and evolution of this major feature of mating systems. Departing from the classical view of monophyly of all forms of self-incompatibility, the current paradigm for the origin of self-incompatibility postulates multiple episodes of recruitment and modification of preexisting genes. In Brassica, the S locus, which regulates sporophytic self-incompatibility, shows homology to a multigene family present both in self-compatible congeners and in groups for which this form of self-incompatibility is atypical. A phylogenetic analysis of S-allele sequences together with homologous sequences that do not cosegregate with self-incompatibility permits dating the change of function that marked the origin of self-incompatibility. A generalized least-squares method is introduced that provides closed-form expressions for estimates and standard errors for function-specific divergence rates and times of divergence among sequences. This analysis suggests that the age of the sporophytic self-incompatibility system expressed in Brassica exceeds species divergence within the genus by four- to fivefold. The extraordinarily high levels of sequence diversity exhibited by S alleles appears to reflect their ancient derivation, with the alternative hypothesis of hypermutability rejected by the analysis.
Genetics 03/1995; 139(2):975-92. · 4.01 Impact Factor
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Heredity 01/1995; 75:405-415. · 4.60 Impact Factor
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ABSTRACT: We study the evolution of the rate of self-fertilization in response to deleterious mutations at multiple loci. Although partial selfing induces associations among loci even in the absence of linkage, associations among mutations at different loci are of a smaller order of magnitude than the mutation rate. Genotypes that carry homozygous lethal mutations in heterozygous form at i loci occur in frequencies of the order (Ti) mu i, in which T denotes the number of viability loci and mu the mutation rate. While associations between mutations at different loci remain small even under inbreeding, each viability locus develops an association with the modifier of the rate of self-fertilization that substantially affects the evolution of the breeding system. Positive associations between enhancers of selfing and haplotypes carrying multiple wild-type alleles and positive associations in heterozygosity between the modifier locus and the viability loci promote evolutionary increases in the rate of self-fertilization.
Theoretical Population Biology 11/1991; 40(2):173-210. · 1.65 Impact Factor
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ABSTRACT: Simple theories for the evolution of breeding systems suggest that the fate of an allele that modifies the rate of self-fertilization hinges only on the degree to which selfing reduces opportunities for outcrossing ("pollen discounting") and the extent of inbreeding depression. These theories predict that outcrossing evolves whenever deleterious mutations have a more severe effect in combination than expected from their individual effects. We study the evolutionary dynamics of a modifier of the rate of self-fertilization in populations subject to complete pollen discounting and recurrent mutations which impair viability at a single locus in diploids and at two loci in haploids. Our analysis indicates that genetic associations arising immediately upon the introduction of a rare modifier allele generate substantial quantitative and qualitative departures from expectation. Higher rates of segregation under selfing in our one-locus diploid model generate positive associations between enhancers of selfing and wild-type viability alleles, which in turn favor the evolution of selfing under a wider range of conditions than expected. Greater opportunities for recombination under outcrossing in our two-locus haploid model generate positive associations between enhancers of outcrossing and wild-type viability alleles. These associations favor the evolution of outcrossing under a wider range of conditions, and introduce the possibility of stable mixed mating systems involving both selfing and outcrossing. Our explicit analysis of genetic associations between loci affecting viability and the rate of self-fertilization indicates that modifiers that enhance the production of offspring with very high (and very low) viability by promoting segregation or recombination develop positive associations with high viability. This advantage of producing extremes can compensate for an initial disadvantage in offspring number.
Theoretical Population Biology 09/1991; 40(1):14-46. · 1.65 Impact Factor
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ABSTRACT: We describe the evolutionary dynamics of a modifier of selfing coevolving with a locus subject to symmetric overdominance in viability under general levels of reduction in pollination success as a consequence of self-fertilization (pollen discounting). Simple models of the evolution of breeding systems that represent inbreeding depression as a constant parameter do not admit the possibility of stable mixed mating systems involving both inbreeding and random mating. Contrary to this expectation, we find that coevolution between a modifier of selfing and a single overdominant locus situated anywhere in the genome can generate evolutionarily attracting mixed mating systems. Two forms of association between the modifier locus and the viability locus promote the evolution of outcrossing. The favored heterozygous genotype at the viability locus develops positive associations with modifier alleles that enhance outcrossing and with the heterozygous genotype at the modifier locus. Associations between outcrossing and high viability evolve immediately upon the introduction of a rare modifier allele, even in the absence of linkage.
Theoretical Population Biology 09/1991; 40(1):47-77. · 1.65 Impact Factor
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M K Uyenoyama
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ABSTRACT: Recent genetic analyses have demonstrated that self-incompatibility in flowering plants derives from the coordinated expression of a system of loci. To address the selective mechanisms through which a genetic system of this kind evolves, I present a three-locus model for the origin of gametophytic self-incompatibility. Conventional models assume that a single locus encodes all physiological effects associated with self-incompatibility and that the viability of offspring depends only on whether they were derived by selfing or outcrossing. My model explicitly represents the genetic determination of offspring viability by a locus subject to symmetrically overdominant selection. Initially, the level of expression of the proto-S locus is insufficient to induce self-incompatibility. Weak gametophytic self-incompatibility arises upon the introduction of a rare allele at an unlinked modifier locus which enhances the expression of the proto-S locus. While conventional models predict that the origin of self-incompatibility requires at least two- to threefold levels of inbreeding depression, I find that the comparatively low levels of inbreeding depression generated by a single overdominant locus can ensure the invasion of an enhancer of self-incompatibility under sufficiently high rates of receipt of self-pollen. Associations among components of the incompatibility system promote the origin of self-incompatibility. Enhancement of heterozygosity at the initially neutral proto-S locus improves offspring viability through associative overdominance. Further, the modifier that enhances the expression of self-incompatibility develops a direct association with heterozygosity at the overdominant viability locus. These results suggest that the evolutionary processes by which incompatibility systems originate may differ significantly from those associated with their breakdown. The genetic mechanism explored here may apply to the evolution of other systems that restrict reproduction, including maternal-fetal incompatibility in mammals.
Genetics 07/1991; 128(2):453-69. · 4.01 Impact Factor
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ABSTRACT: We study the conditions under which a rare allele that modifies the relative rates of meiotic reproduction and apomixis increases in a population in which meiotic reproduction entails selfing as well as random outcrossing. A distinct locus, at which mutation maintains alleles that are lethal in homozygous form, determines viability. We find that low viability of carriers of the lethal alleles, high rates of selfing, dominance of the introduced modifier allele, and lower rates of recombination promote the evolution of meiosis. Meiotic reproduction can evolve even in the absence of linkage between the modifier and the viability locus. The adaptive value of meiotic reproduction depends on the relative viabilities of offspring derived by meiosis and by apomixis, and on associations between the modifier and the viability locus. Meiotic reproduction, particularly under selfing, generates more diverse offspring, including those with very high and very low viability. Elimination of offspring with low viability generates positive associations between enhancers of meiotic reproduction and high viability. In addition, partial selfing generates positive associations in heterozygosity (identity disequilibrium) between the modifier and the viability locus, even in the absence of linkage. The two kinds of associations together can compensate for initial reductions in mean offspring viability under meiotic reproduction.
Genetics 01/1990; 123(4):873-85. · 4.01 Impact Factor
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M K Uyenoyama
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ABSTRACT: Conditions for the origin of partial sporophytic self-incompatibility (SSI) are obtained from two quantitative models, which differ with respect to the determination of offspring viability. Offspring viability depends solely on the source (self or nonself) of the fertilizing pollen in the first model, which describes changes only at a primitive S-locus itself. Two loci evolve in the second model: overdominant viability selection maintains an arbitrary number of alleles at one locus, with SSI under the control of a separate locus. In both cases, the origin of SSI requires that the relative change in the numbers of offspring derived by the two reproductive modes compensate for the twofold cost of outcrossing. In the first model studied, the viability of inbred offspring fully determines the relative change in the numbers of inbred and outbred offspring produced. In the second model, the relative change in offspring numbers depends in addition on associations between the S-locus and the viability locus. Because these two-locus associations are comparable in magnitude to the differences between the viabilities of inbred and outbred offspring, SSI can arise under less restrictive conditions than expected from the one-locus model. Greater allelic multiplicity at the viability locus facilitates the origin of SSI by reducing the relative viability of inbred offspring. Tight linkage between the S-locus and the viability locus and high rates of receipt of self-pollen promote the generation and maintenance of associations between the S-locus and the viability locus. In populations in which more than two viability alleles are maintained, the active S-allele can invade even in the absence of linkage with the viability locus. The present study establishes that incompatibility systems can arise in response to identity disequilibrium between a modifier of incompatibility and a locus subject to overdominant viability selection; in particular, compensation for the twofold cost of outcrossing does not require preexisting gametic level disequilibria.
Theoretical Population Biology 01/1990; 36(3):339-65. · 1.65 Impact Factor
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M K Uyenoyama
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ABSTRACT: A quantitative model is developed to explore the effects of prezygotic and postzygotic incompatibility on the origin and maintenance of associations between the major histocompatibility complex (MHC) and the t-complex in the mouse. Incompatibility is represented by a reduction in the rate of conception or gestation of offspring derived from sperm bearing MHC antigens in common with the mother. Incompatibility encourages the evolution of associations from a state of complete independence between the two complexes by promoting the invasion of all novel antigens, including those that exhibit associations with the t-complex. Incompatibility can modify the relative numbers of antigens associated with each haplotype by actively promoting the exclusion or invasion of recombinants that bear formerly +-specific or t-specific antigens on the alternative haplotype. The results of the analysis indicate that the state of complete independence between the MHC and the t-complex is not preserved over evolutionary time in the presence of incompatibility. Further, the expression of incompatibility maintains fully associated states that include a single antigen associated with the t-haplotype and up to three to five antigens associated with the +-haplotype within a single population.
Genetics 02/1989; 121(1):139-51. · 4.01 Impact Factor
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M K Uyenoyama
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ABSTRACT: Selective pressures imposed by high complementarity associations between the major histocompatibility complex (MHC) and the t-complex on a locus that modifies the expression of prezygotic and postzygotic incompatibility are investigated through the analysis of a quantitative model. Sharing of MHC antigens between mates or between mother and offspring elicits weak inhibition of conception or gestation. In the presence of high complementarity associations between the MHC and the t-complex, weak incompatibility depresses the mean fitness of the population. Nevertheless, natural selection favors the enhancement of the expression of incompatibility if the number of antigens associated with the +-haplotype exceeds the number associated with the t-haplotype by a sufficient margin. Under absolute linkage between the modifier locus and the t-complex, the number associated with the +-haplotype need only be greater than the number associated with the t-haplotype. In the absence of linkage, a twofold difference is sufficient to ensure the initial increase of modifier alleles that intensify the expression of incompatibility.
Genetics 02/1989; 121(1):153-61. · 4.01 Impact Factor
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ABSTRACT: Nuclear and cytoplasmic determinants jointly influence the sex ratio in several organisms. A mathematical model of a maternally inherited extra-chromosomal agent that affects the fitness of its carriers and distorts the sex ratio in their broods is analyzed. The agent is transmitted through the cytoplasm from mother to daughter, or it may pass contagiously among females of the same generation. It is shown that under natural selection the deviation between the population sex ratio and Fisher's optimum value evolves to a minimum.
Theoretical Population Biology 01/1979; 14(3):471-97. · 1.65 Impact Factor
