A Bayesian Approach to Inferring Rates of Selfing and Locus-Specific Mutation.
ABSTRACT: We present a Bayesian method for characterizing the mating system of populations reproducing through a mixture of self-fertilization and random outcrossing. Our method uses patterns of genetic variation across the genome as a basis for inference about reproduction under pure hermaphroditism, gynodioecy, and a model developed to describe the self-fertilizing killifish Kryptolebias marmoratus. We extend the standard coalescence model to accommodate these mating systems, accounting explicitly for multilocus identity disequilibrium, inbreeding depression, and variation in fertility among mating types. We incorporate the Ewens sampling formula (ESF) under the infinite-alleles model of mutation to obtain a novel expression for the likelihood of mating system parameters. Our Markov chain Monte Carlo (MCMC) algorithm assigns locus-specific mutation rates, drawn from a common mutation rate distribution that is itself estimated from the data using a Dirichlet process prior model. Our sampler is designed to accommodate additional information, including observations pertaining to the sex ratio, the intensity of inbreeding depression, and other aspects of reproduction. It can provide joint posterior distributions for the population-wide proportion of uniparental individuals, locus-specific mutation rates, and the number of generations since the most recent outcrossing event for each sampled individual. Further, estimation of all basic parameters of a given model permits estimation of functions of those parameters, including the proportion of the gene pool contributed by each sex and relative effective numbers.
Project description:There is a long-recognized association in plants between small stature and selfing, and large stature and outcrossing. Inbreeding depression is central to several hypotheses for this association, but differences in the evolutionary dynamics of inbreeding depression associated with differences in stature are rarely considered. Here, we propose and test the Phi model of plant mating system evolution, which assumes that the per-generation mutation rate of a plant is a function of the number of mitoses (Phi) that occur from zygote to gamete, and predicts fundamental differences between low-Phi (small-statured) and high-Phi (large-statured) plants in the outcomes of the joint evolution of outcrossing rate and inbreeding depression. Using a large dataset of published population genetic studies of angiosperms and conifers, we compute fitted values of inbreeding depression and deleterious mutation rates for small- and large-statured plants. Consistent with our Phi model, we find that populations of small-statured plants exhibit a range of mating systems, significantly lower mutation rates, and intermediate inbreeding depression, while large-statured plants exhibit very high mutation rates and the maximum inbreeding depression of unity. These results indicate that (i) inbred progeny typically observed in large-statured plant populations are completely lost prior to maturity in nearly all populations; (ii) evolutionary shifts from outcrossing to selfing are generally not possible in large-statured species, rather, large-statured species are more likely to evolve mating systems that avoid selfing such as self-incompatibility and dioecy; (iii) destabilization of the mating system-high selfing rate with high-inbreeding depression-might be a common occurrence in large-statured species; and (iv) large-statured species in fragmented populations might be at higher risk of extinction than previously thought. Our results help to unify and simplify a large and diverse field of research, and serve to emphasize the importance that developmental and genetic constraints play in the evolution of plant mating systems.
Project description:Understanding the factors that shape macroevolutionary patterns in functional traits is a central goal of evolutionary biology. Alternative strategies of sexual reproduction (inbreeding vs. outcrossing) have divergent effects on population genetic structure and could thereby broadly influence trait evolution. However, the broader evolutionary consequences of mating system transitions remain poorly understood, with the exception of traits related to reproduction itself (e.g., pollination). Across a phylogeny of 56 wild species of Solanaceae (nightshades), we show here that the repeated, unidirectional transition from ancestral self-incompatibility (obligate outcrossing) to self-compatibility (increased inbreeding) leads to the evolution of an inducible (vs. constitutive) strategy of plant resistance to herbivores. We demonstrate that inducible and constitutive defense strategies represent evolutionary alternatives and that the magnitude of the resulting macroevolutionary tradeoff is dependent on the mating system. Loss of self-incompatibility is also associated with the evolution of increased specificity in induced plant resistance. We conclude that the evolution of sexual reproductive variation may have profound effects on plant-herbivore interactions, suggesting a new hypothesis for the evolution of two primary strategies of plant defense.
Project description:High inbreeding depression is thought to be one of the major factors preventing evolutionary transitions in hermaphroditic plants from self-incompatibility (SI) and outcrossing toward self-compatibility (SC) and selfing. However, when selfing does evolve, inbreeding depression can be quickly purged, allowing the evolution of complete self-fertilization. In contrast, populations that show intermediate selfing rates (a mixed-mating system) typically show levels of inbreeding depression similar to those in outcrossing species, suggesting that selection against inbreeding might be responsible for preventing the transition toward complete self-fertilization. By implication, crosses among populations should reveal patterns of heterosis for mixed-mating populations that are similar to those expected for outcrossing populations. Using hand-pollination crosses, we compared levels of inbreeding depression and heterosis between populations of Linaria cavanillesii (Plantaginaceae), a perennial herb showing contrasting mating systems. The SI population showed high inbreeding depression, whereas the SC population displaying mixed mating showed no inbreeding depression. In contrast, we found that heterosis based on between-population crosses was similar for SI and SC populations. Our results are consistent with the rapid purging of inbreeding depression in the derived SC population, despite the persistence of mixed mating. However, the maintenance of outcrossing after a transition to SC is inconsistent with the prediction that populations that have purged their inbreeding depression should evolve toward complete selfing, suggesting that the transition to SC in L. cavanillesii has been recent. SC in L. cavanillesii thus exemplifies a situation in which the mating system is likely not at an equilibrium with inbreeding depression.
Project description:Global climate change affects natural populations of many species by increasing the average temperature and the frequency of extreme weather events (e.g. summer heat waves). The ability of organisms to cope with these environmental changes can, however, depend on their genetic properties. For instance, genetic load owing to inbreeding could alter organisms' responses to climate change-mediated environmental changes but such effects are often overlooked. We investigated the effects of an experimental heat wave (25°C versus 15°C) on life history (reproduction, size) and constitutive immune defence traits (phenoloxidase-like and antibacterial activity of haemolymph) in relation to inbreeding by manipulating the mating type (outcrossing, self-fertilization) in two populations of a hermaphroditic freshwater snail, Lymnaea stagnalis. High temperature increased reproduction and size of snails but impaired their immune function. In one of the two study populations, inbreeding reduced reproductive output of snails indicating inbreeding depression. Furthermore, this effect did not depend on the temperature snails were exposed to. Our results suggest that L. stagnalis snails can be negatively affected by inbreeding but it may not alter their responses to heat waves.
Project description:Saccharomyces paradoxus is the closest known relative of the well-known S. cerevisiae and an attractive model organism for population genetic and genomic studies. Here we characterize a set of 28 wild isolates from a 10-km(2) sampling area in southern England. All 28 isolates are homothallic (capable of mating-type switching) and wild type with respect to nutrient requirements. Nine wild isolates and two lab strains of S. paradoxus were surveyed for sequence variation at six loci totaling 7 kb, and all 28 wild isolates were then genotyped at seven polymorphic loci. These data were used to calculate nucleotide diversity and number of segregating sites in S. paradoxus and to investigate geographic differentiation, population structure, and linkage disequilibrium. Synonymous site diversity is approximately 0.3%. Extensive incompatibilities between gene genealogies indicate frequent recombination between unlinked loci, but there is no evidence of recombination within genes. Some localized clonal growth is apparent. The frequency of outcrossing relative to inbreeding is estimated at 1.1% on the basis of heterozygosity. Thus, all three modes of reproduction known in the lab (clonal replication, inbreeding, and outcrossing) have been important in molding genetic variation in this species.
Project description:Cryptococcus neoformans is a pathogenic basidiomycetous fungus that engages in outcrossing, inbreeding, and selfing forms of unisexual reproduction as well as canonical sexual reproduction between opposite mating types. Long thought to be clonal, >99% of sampled environmental and clinical isolates of C. neoformans are MAT?, limiting the frequency of opposite mating-type sexual reproduction. Sexual reproduction allows eukaryotic organisms to exchange genetic information and shuffle their genomes to avoid the irreversible accumulation of deleterious changes that occur in asexual populations, known as Muller's ratchet. We tested whether unisexual reproduction, which dispenses with the requirement for an opposite mating-type partner, is able to purge the genome of deleterious mutations. We report that the unisexual cycle can restore mutant strains of C. neoformans to wild-type genotype and phenotype, including prototrophy and growth rate. Furthermore, the unisexual cycle allows attenuated strains to purge deleterious mutations and produce progeny that are returned to wild-type virulence. Our results show that unisexual populations of C. neoformans are able to avoid Muller's ratchet and loss of fitness through a unisexual reproduction cycle involving ?-? cell fusion, nuclear fusion, and meiosis. Similar types of unisexual reproduction may operate in other pathogenic and saprobic eukaryotic taxa.
Project description:Pollen movements and mating patterns are key features that influence population genetic structure. When gene flow is low, small populations are prone to increased genetic drift and inbreeding, but naturally disjunct species may have features that reduce inbreeding and contribute to their persistence despite genetic isolation. Using microsatellite loci, we investigated outcrossing levels, family mating parameters, pollen dispersal, and spatial genetic structure in three populations of Hakea oldfieldii, a fire-sensitive shrub with naturally disjunct, isolated populations prone to reduction in size and extinction following fires. We mapped and genotyped a sample of 102 plants from a large population, and all plants from two smaller populations (28 and 20 individuals), and genotyped 158-210 progeny from each population. We found high outcrossing despite the possibility of geitonogamous pollination, small amounts of biparental inbreeding, a limited number of successful pollen parents within populations, and significant correlated paternity. The number of pollen parents for each seed parent was moderate. There was low but significant spatial genetic structure up to 10 m around plants, but the majority of successful pollen came from outside this area including substantial proportions from distant plants within populations. Seed production varied among seven populations investigated but was not correlated with census population size. We suggest there may be a mechanism to prevent self-pollination in H. oldfieldii and that high outcrossing and pollen dispersal within populations would promote genetic diversity among the relatively small amount of seed stored in the canopy. These features of the mating system would contribute to the persistence of genetically isolated populations prone to fluctuations in size.
Project description:The evolution of sociality in spiders is associated with female bias, reproductive skew and an inbreeding mating system, factors that cause a reduction in effective population size and increase effects of genetic drift. These factors act to decrease the effectiveness of selection, thereby increasing the fixation probability of deleterious mutations. Comparative studies of closely related species with contrasting social traits and mating systems provide the opportunity to test consequences of low effective population size on the effectiveness of selection empirically. We used phylogenetic analyses of three inbred social spider species and seven outcrossing subsocial species of the genus Stegodyphus, and compared dN/dS ratios and codon usage bias between social Inbreeding and subsocial outcrossing mating systems to assess the effectiveness of selection. The overall results do not differ significantly between the social inbreeding and outcrossing species, but suggest a tendency for lower codon usage bias and higher dN/dS ratios in the social inbreeding species compared with their outcrossing congeners. The differences in dN/dS ratio and codon usage bias between social and subsocial species are modest but consistent with theoretical expectations of reduced effectiveness of selection in species with relatively low effective population size. The modest differences are consistent with relatively recent evolution of social mating systems. Additionally, the short terminal branches and lack of speciation of the social lineages, together with low genetic diversity lend support for the transient state of permanent sociality in spiders.
Project description:The population outcrossing rate (t) and adult inbreeding coefficient (F) are key parameters in mating system evolution. The magnitude of inbreeding depression as expressed in the field can be estimated given t and F via the method of Ritland (1990). For a given total sample size, the optimal design for the joint estimation of t and F requires sampling large numbers of families (100-400) with fewer offspring (1-4) per family. Unfortunately, the standard inference procedure (MLTR) yields significantly biased estimates for t and F when family sizes are small and maternal genotypes are unknown (a common occurrence when sampling natural populations). Here, we present a Bayesian method implemented in the program BORICE (Bayesian Outcrossing Rate and Inbreeding Coefficient Estimation) that effectively estimates t and F when family sizes are small and maternal genotype information is lacking. BORICE should enable wider use of the Ritland approach for field-based estimates of inbreeding depression. As proof of concept, we estimate t and F in a natural population of Mimulus guttatus. In addition, we describe how individual maternal inbreeding histories inferred by BORICE may prove useful in studies of inbreeding and its consequences.
Project description:Studying associations between mating system parameters and fitness in natural populations of trees advances our understanding of how local environments affect seed quality, and thereby helps to predict when inbreeding or multiple paternities should impact on fitness. Indeed, for species that demonstrate inbreeding avoidance, multiple paternities (i.e. the number of male parents per half-sib family) should still vary and regulate fitness more than inbreeding--named here as the 'constrained inbreeding hypothesis'. We test this hypothesis in Eucalyptus gracilis, a predominantly insect-pollinated tree. Fifty-eight open-pollinated progeny arrays were collected from trees in three populations. Progeny were planted in a reciprocal transplant trial. Fitness was measured by family establishment rates. We genotyped all trees and their progeny at eight microsatellite loci. Planting site had a strong effect on fitness, but seed provenance and seed provenance × planting site did not. Populations had comparable mating system parameters and were generally outcrossed, experienced low biparental inbreeding and high levels of multiple paternity. As predicted, seed families that had more multiple paternities also had higher fitness, and no fitness-inbreeding correlations were detected. Demonstrating that fitness was most affected by multiple paternities rather than inbreeding, we provide evidence supporting the constrained inbreeding hypothesis; i.e. that multiple paternity may impact on fitness over and above that of inbreeding, particularly for preferentially outcrossing trees at life stages beyond seed development.