Natural populations of guppies were subjected to an episode of directional selection that mimicked natural processes. The resulting rate of evolution of age and size at maturity was similar to rates typically obtained for traits subjected to artificial selection in laboratory settings and up to seven orders of magnitude greater than rates inferred from the paleontological record. Male traits evolved more rapidly than female traits largely because males had more genetic variation upon which natural selection could act. These results are considered in light of the ongoing debate about the importance of natural selection versus other processes in the paleontological record of evolution.
Deleterious mutations are of fundamental importance to all aspects of organismal biology. Evolutionary geneticists have expended tremendous effort to estimate the genome-wide rate of mutation and the effects of new mutations on fitness, but the degree to which genomic mutational properties vary within and between taxa is largely unknown, particularly in multicellular organisms. Beginning with two highly inbred strains from each of three species in the nematode family Rhabditidae (Caenorhabditis briggsae, Caenorhabditis elegans, and Oscheius myriophila), we allowed mutations to accumulate in the relative absence of natural selection for 200 generations. We document significant variation in the rate of decay of fitness because of new mutations between strains and between species. Estimates of the per-generation mutational decay of fitness were very consistent within strains between assays 100 generations apart. Rate of mutational decay in fitness was positively associated with genomic mutation rate and negatively associated with average mutational effect. These results provide unambiguous experimental evidence for substantial variation in genome-wide properties of mutation both within and between species and reinforce conclusions from previous experiments that the cumulative effects on fitness of new mutations can differ markedly among related taxa.Caenorhabditis briggsae ͉ Caenorhabditis elegans ͉ deleterious mutation ͉ mutation accumulation ͉ Oscheius myriophila F ew topics in evolutionary biology have generated as much controversy in recent years as spontaneous mutation, considered at the level of the entire genome (1-4). It is widely accepted that the great majority of new mutations are either neutral or deleterious (refs. 1 and 5-7; also see refs. 3 and 8-13), and the importance of deleterious mutations to a wide variety of biological processes and phenomena is well appreciated (7). The source of the controversy stems from uncertainty in the rate at which new mutations accrue in the genome and the distribution of effects of those mutations on fitness.Beginning in the early 1960s, Mukai, Ohnishi, and their colleagues (14-18) conducted several large mutation accumulation (MA) experiments with Drosophila melanogaster that were designed to estimate the rate and average effect of new mutations on fitness. By the early 1970s, the results seemed clear: averaged over experiments, egg-to-adult viability declined rapidly, on the order of 1% per genome per generation, with the implication that the diploid genomic mutation rate (U) was on the order of 0.6 per generation or greater and the average homozygous effect on fitness of a new mutation (2a ) was Ϸ0.05 or less. The typical newborn fly was thus expected to harbor one new mutation that could be expected to reduce its viability by Ϸ5% when homozygous.Several additional lines of evidence supported the results from the early f ly MA experiments. First, the considerable inbreeding depression in Drosophila implied either a high rate of deleterious mutation or considerable...
As the ultimate source of genetic variation, spontaneous mutation is essential to evolutionary change. Theoretical studies over several decades have revealed the dependence of evolutionary consequences of mutation on specific mutational properties, including genomic mutation rates, U, and the effects of newly arising mutations on individual fitness, s. The recent resurgence of empirical effort to infer these properties for diverse organisms has not achieved consensus. Estimates, which have been obtained by methods that assume mutations are unidirectional in their effects on fitness, are imprecise. Both because a general approach must allow for occurrence of fitness-enhancing mutations, even if these are rare, and because recent evidence demands it, we present a new method for inferring mutational parameters. For the distribution of mutational effects, we retain Keightley's assumption of the gamma distribution, to take advantage of the flexibility of its shape. Because the conventional gamma is one sided, restricting it to unidirectional effects, we include an additional parameter, rho, as an amount it is displaced from zero. Estimation is accomplished by Markov chain Monte Carlo maximum likelihood. Through a limited set of simulations, we verify the accuracy of this approach. We apply it to analyze data on two reproductive fitness components from a 17-generation mutation-accumulation study of a Columbia accession of Arabidopsis thaliana in which 40 lines sampled in three generations were assayed simultaneously. For these traits, U approximately/= 0.1-0.2, with distributions of mutational effects broadly spanning zero, such that roughly half the mutations reduce reproductive fitness. One evolutionary consequence of these results is lower extinction risks of small populations of A. thaliana than expected from the process of mutational meltdown. A comprehensive view of the evolutionary consequences of mutation will depend on quantitatively accounting for fitness-enhancing, as well as fitness-reducing, mutations.
A key problem in evolutionary biology has been distinguishing the contributions of current and historical processes to the maintenance of genetic variation. Because alleles at self-recognition genes are under balancing selection, they exhibit extended residence times in populations and thus may provide unique insight into population demographic history. However, evidence for balancing selection and extended residence times has almost exclusively depended on identification of transspecific polymorphisms; polymorphisms retained in populations through speciation events. We present a broadly applicable approach for detecting balancing selection and apply it to the b1 mating type gene in the mushroom fungus Coprinus cinereus. The comparison of neutral molecular variation within and between allelic classes was used to directly estimate the strength of balancing selection. Different allelic classes are defined as encoding different mating compatibility types and are thus potentially subject to balancing selection. Variation within an allelic class, where all alleles have the same mating compatibility type, provided an internal standard of neutral evolution. Mating compatibility in this organism is determined by the complex A mating type locus, and b1 is one of several redundantly functioning genes. Consequently, we conducted numerical simulations of a model with two subloci and varying levels of recombination to show that balancing selection should operate at each sublocus. Empirical data show that strong balancing selection has indeed occurred at the b1 locus. The widespread geographic distribution of identical b1 alleles suggests that their association with differing A mating types is the result of recent recombination events.
Mutations are the ultimate source of genetic diversity and their contributions to evolutionary process depend critically on their rate and their effects on traits, notably fitness. Mutation rate and mutation effect can be measured simultaneously through the use of mutation accumulation lines, and previous mutation accumulation studies measuring these parameters have been performed in laboratory conditions. However, estimation of mutation parameters for fitness in wild populations requires assays in environments where mutations are exposed to natural selection and natural environmental variation. Here we quantify mutation parameters in both the wild and greenhouse environments using 100 25th generation Arabidopsis thaliana mutation accumulation lines. We found significantly greater mutational variance and a higher mutation rate for fitness under field conditions relative to greenhouse conditions. However, our field estimates were low when scaled to natural environmental variation. Many of the mutation accumulation lines have increased fitness, counter to the expectation that nearly all mutations decrease fitness. A high mutation rate and a low mutational contribution to phenotypic variation may explain observed levels of natural genetic variation.Our findings indicate that mutation parameters are not fixed, but are variables whose values may reflect the specific environment in which mutations are tested. K E Y W O R D S :Beneficial mutations, mutation accumulation lines, mutation effect, mutation rate.
The additive genetic variance with respect to absolute fitness, V A (W), divided by mean absolute fitness, W, sets the rate of ongoing adaptation. Fisher's key insight yielding this quantitative prediction of adaptive evolution, known as the Fundamental Theorem of Natural Selection, is well appreciated by evolutionists. Nevertheless, extremely scant information about V A (W) is available for natural populations. Consequently, the capacity for fitness increase via natural selection is unknown. Particularly in the current context of rapid environmental change, which is likely to reduce fitness directly and, consequently, the size and persistence of populations, the urgency of advancing understanding of immediate adaptive capacity is extreme. We here explore reasons for the dearth of empirical information about V A (W), despite its theoretical renown and critical evolutionary role. Of these reasons, we suggest that expectations that V A (W) is negligible, in general, together with severe statistical challenges of estimating it, may largely account for the limited empirical emphasis on it. To develop insight into the dynamics of V A (W) in a changing environment, we have conducted individual-based genetically explicit simulations. We show that, as optimizing selection on a trait changes steadily over generations, V A (W) can grow considerably, supporting more rapid adaptation than would the V A (W) of the base population. We call for direct evaluation of V A (W) and W in support of prediction of rates adaptive evolution, and we advocate for the use of aster modeling as a rigorous basis for achieving this goal.
Evolution of local adaptation depends critically on the level of gene flow, which, in plants, can be due to either pollen or seed dispersal. Using analytical predictions and individual‐centred simulations, we investigate the specific influence of seed and pollen dispersal on local adaptation in plant populations growing in patchy heterogeneous landscapes. We study the evolution of a polygenic trait subject to stabilizing selection within populations, but divergent selection between populations. Deviations from linkage equilibrium and Hardy–Weinberg equilibrium make different contributions to genotypic variance depending on the dispersal mode. Local genotypic variance, differentiation between populations and genetic load vary with the rate of gene flow but are similar for seed and pollen dispersal, unless the landscape is very heterogeneous. In this case, genetic load is higher in the case of pollen dispersal, which appears to be due to differences in the distribution of genotypic values before selection.
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