Meiotic drivers are genetic variants that selfishly manipulate the production of gametes to increase their own rate of transmission, often to the detriment of the rest of the genome and the individual that carries them. This genomic conflict potentially occurs whenever a diploid organism produces a haploid stage, and can have profound evolutionary impacts on gametogenesis, fertility, individual behaviour, mating system, population survival, and reproductive isolation. Multiple research teams are developing artificial drive systems for pest control, utilising the transmission advantage of drive to alter or exterminate target species. Here, we review current knowledge of how natural drive systems function, how drivers spread through natural populations, and the factors that limit their invasion. Trends Box Both naturally occurring and synthetic "meiotic drivers" violate Mendel's law of equal segregation and can rapidly spread through populations even when they reduce the fitness of individuals carrying them. Synthetic drivers are being developed to spread desirable genes in natural populations of target species. How ecology influences the population dynamics of meiotic drivers is important for predicting the success of synthetic drive elements. An enduring puzzle concerns why some meiotic drivers persist at stable, intermediate frequencies rather than sweeping to fixation. Drivers can have a wide range of consequences from extinction to changes in mating system. preferentially associating with and moving toward the egg pole at Meiosis I) will be 75 transmitted to more than half of the maturing eggs. Although this bias does not necessarily 76 reduce the production of eggs (as only one egg matures per meiosis), the fitness of other 77 alleles at the same locus, that do not bias transmission, and alleles linked to them, is 78 reduced. Such meiotic drivers could reduce the fitness of individuals that carry them, if the 79 driving variant is genetically linked to deleterious mutations or has deleterious pleiotropic 80 effects. 81Male meiotic drive takes multiple forms -some at least partially meiotic, some entirely 82 post-meiotic -but all involve a driving element that prevents maturation or function of 83 sperm that do not contain it. Because haploid sperm within a single ejaculate compete to 84 fertilize the same pool of eggs, disabling non-carrier sperm results in transmission of the 85 driving element to more than half of the functional gametes and resulting offspring ([5], Box 86 1). However, disabling non-carrier sperm often reduces fertility [6]. 87Spore drive in fungi, in which the products of meiosis are packaged together in an ascus, 88 operates via similar mechanisms. Spores with one haploid genotype will kill or disable 89 spores of the alternative haplotype ([7], Box 1). If spores disperse long distances sibling 90 spores are unlikely to compete and killing them will not increase the killer's fitness. 91However, spore killing can be beneficial if there is local resource competition. 92Excit...
Female meiotic drive, in which paired chromosomes compete for access to the egg, is a potentially powerful but rarely documented evolutionary force. In interspecific monkeyflower (Mimulus) hybrids, a driving M. guttatus allele (D) exhibits a 98:2 transmission advantage via female meiosis. We show that extreme interspecific drive is most likely caused by divergence in centromere-associated repeat domains and document cytogenetic and functional polymorphism for drive within a population of M. guttatus. In conspecific crosses, D had a 58:42 transmission advantage over nondriving alternative alleles. However, individuals homozygous for the driving allele suffered reduced pollen viability. These fitness effects and molecular population genetic data suggest that balancing selection prevents the fixation or loss of D and that selfish chromosomal transmission may affect both individual fitness and population genetic load.
Abstract. The genetic basis of species differences provides insight into the mode and tempo of phenotypic divergence. We investigate the genetic basis of floral differences between two closely related plant taxa with highly divergent mating systems, Mimulus guttatus (large-flowered outcrosser) and M. nasutus (small-flowered selfer). We had previously constructed a framework genetic linkage map of the hybrid genome containing 174 markers spanning approximately 1800 cM on 14 linkage groups. In this study, we analyze the genetics of 16 floral, reproductive, and vegetative characters measured in a large segregating M. nasutus ϫ M. guttatus F 2 population (N ϭ 526) and in replicates of the parental lines and F 1 hybrids. Phenotypic analyses reveal strong genetic correlations among floral traits and epistatic breakdown of male and female fertility traits in the F 2 hybrids. We use multitrait composite interval mapping to jointly locate and characterize quantitative trait loci (QTLs) underlying interspecific differences in seven floral traits. We identified 24 floral QTLs, most of which affected multiple traits. The large number of QTLs affecting each trait (mean ϭ 13, range ϭ 11-15) indicates a strikingly polygenic basis for floral divergence in this system. In general, QTL effects are small relative to both interspecific differences and environmental variation within genotypes, ruling out QTLs of major effect as contributors to floral divergence between M. guttatus and M. nasutus. QTLs show no pattern of directional dominance. Floral characters associated with pollinator attraction (corolla width) and self-pollen deposition (stigma-anther distance) share several pleiotropic or linked QTLs, but unshared QTLs may have allowed selfing to evolve independently from flower size. We discuss the polygenic nature of divergence between M. nasutus and M. guttatus in light of theoretical work on the evolution of selfing, genetics of adaptation, and maintenance of variation within populations.
Ecological factors that reduce the effectiveness of cross-pollination are likely to play a role in the frequent evolution of routine self-fertilization in flowering plants. However, we lack empirical evidence linking the reproductive assurance value of selfing in poor pollination environments to evolutionary shifts in mating system. Here, we investigated the adaptive significance of prior selfing in the polymorphic annual plant Arenaria uniflora (Caryophyllaceae), in which selfer populations occur only in areas of range overlap with congener A. glabra. To examine the hypothesis that secondary contact between the two species contributed to the evolution and maintenance of selfing, we used field competition experiments and controlled hand-pollinations to measure the female fitness consequences of pollinator-mediated interspecific interactions. Uniformly high fruit set by selfers in the naturally pollinated field arrays confirmed the reproductive assurance value of selfing, whereas substantial reductions in outcrosser fruit set (15%) and total seed production (20-35%) in the presence of A. glabra demonstrated that pollinator-mediated interactions can provide strong selection for self-pollination. Heterospecific pollen transfer, rather than competition for pollinator service, appears to be the primary mechanism of pollinator-mediated competition in Arenaria. Premating barriers to hybridization between outcrossers and A. glabra are extremely weak. The production of a few inviable hybrid seeds after heterospecific pollination and intermediate seed set after mixed pollinations indicates that A. glabra pollen can usurp A. uniflora ovules. Thus, any visit to A. uniflora by shared pollinators carries a potential female fitness cost. Moreover, patterns of fruit set and seed set in the competition arrays relative to controls were consistent with the receipt of mixed pollen loads, rather than a lack of pollinator visits. Competition through pollen transfer favors preemptive self-pollination and may be responsible for the evolution of a highly reduced floral morphology in A. uniflora selfers as well as their current geographical distribution.
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