Genetic Variation For Fitness Research Articles

The evolution of compensation to herbivory in scarlet gilia, Ipomopsis aggregata: herbivore-imposed natural selection and the quantitative genetics of tolerance.

Tolerance is the ability of plants to maintain fitness after experiencing herbivore damage. We investigated scarlet gilia tolerance to browsing in the framework of phenotypic plasticity using both an operational and candidate trait approach. Individuals from full-sib families were split into an artificial clipping treatment, a natural-damage treatment, or left as controls. We tested for genetic variation in tolerance by evaluating family x herbivory treatment interactions on fitness in a mixed model analysis of variance. In addition, we used selection analyses to assess the function of flowering phenology and compensatory regrowth (via branch production) as candidate tolerance traits. We found a strong detrimental fitness effect of browsing and considerable variation among sire half-sib families in levels of tolerance (25% to 63% of the fitness of controls). There was no evidence of overcompensation at either the population or family level and no additive genetic variation in operationally defined tolerance. Phenotypic selection analyses provide evidence that early flowering and compensatory regrowth function as tolerance characters. We found strong linear and correlational selection for early flowering and increased branch production for damaged plants and linear selection for apical dominance (reduced branchiness) and early flowering in control plants. Moreover, reduced phenological delay and increased plasticity in branch production were correlated with tolerance. We detected significant additive genetic variation in flowering phenology in both treatments and a positive genetic correlation between the phenology of control and damaged plants. We found significant additive genetic variation in branch production in undamaged and naturally damaged plants, but not in clipped plants. Damaged plants exhibited marginally significant additive genetic variance in fitness, although its heritability was very low (approximately 3.6%). We failed to find additive genetic variation in the fitness of control plants. Our results suggest that tolerance traits are under herbivore-imposed natural selection in this population, but that responses to selection are limited by available genetic variation and selective constraints.

THE EVOLUTION OF COMPENSATION TO HERBIVORY IN SCARLET GILIA, IPOMOPSIS AGGREGATA: HERBIVORE-IMPOSED NATURAL SELECTION AND THE QUANTITATIVE GENETICS OF TOLERANCE

Tolerance is the ability of plants to maintain fitness after experiencing herbivore damage. We investigated scarlet gilia tolerance to browsing in the framework of phenotypic plasticity using both an operational and candidate trait approach. Individuals from full-sib families were split into an artificial clipping treatment, a natural-damage treatment, or left as controls. We tested for genetic variation in tolerance by evaluating family × herbivory treatment interactions on fitness in a mixed model analysis of variance. In addition, we used selection analyses to assess the function of flowering phenology and compensatory regrowth (via branch production) as candidate tolerance traits. We found a strong detrimental fitness effect of browsing and considerable variation among sire half-sib families in levels of tolerance (25% to 63% of the fitness of controls). There was no evidence of overcompensation at either the population or family level and no additive genetic variation in operationally defined tolerance. Phenotypic selection analyses provide evidence that early flowering and compensatory regrowth function as tolerance characters. We found strong linear and correlational selection for early flowering and increased branch production for damaged plants and linear selection for apical dominance (reduced branchiness) and early flowering in control plants. Moreover, reduced phenological delay and increased plasticity in branch production were correlated with tolerance. We detected significant additive genetic variation in flowering phenology in both treatments and a positive genetic correlation between the phenology of control and damaged plants. We found significant additive genetic variation in branch production in undamaged and naturally damaged plants, but not in clipped plants. Damaged plants exhibited marginally significant additive genetic variance in fitness, although its heritability was very low (∼ 3.6%). We failed to find additive genetic variation in the fitness of control plants. Our results suggest that tolerance traits are under herbivore-imposed natural selection in this population, but that responses to selection are limited by available genetic variation and selective constraints.Corresponding Editor: J. Conner

Characterization of Deleterious Mutations in Outcrossing Populations

Deng and Lynch recently proposed estimating the rate and effects of deleterious genomic mutations from changes in the mean and genetic variance of fitness upon selfing/outcrossing in outcrossing/highly selfing populations. The utility of our original estimation approach is limited in outcrossing populations, since selfing may not always be feasible. Here we extend the approach to any form of inbreeding in outcrossing populations. By simulations, the statistical properties of the estimation under a common form of inbreeding (sib mating) are investigated under a range of biologically plausible situations. The efficiencies of different degrees of inbreeding and two different experimental designs of estimation are also investigated. We found that estimation using the total genetic variation in the inbred generation is generally more efficient than employing the genetic variation among the mean of inbred families, and that higher degree of inbreeding employed in experiments yields higher power for estimation. The simulation results of the magnitude and direction of estimation bias under variable or epistatic mutation effects may provide a basis for accurate inferences of deleterious mutations. Simulations accounting for environmental variance of fitness suggest that, under full-sib mating, our extension can achieve reasonably well an estimation with sample sizes of only approximately 2000-3000.

On the contribution of deleterious alleles to fitness variance in natural populations of Drosophila.

I have studied the consequences of habitat patchiness on the persistence times of deleterious alleles in a random mating population. Results based on computer simulations and supported by analytical approximations suggest that deleterious alleles remain approximately 1/(1-2FST) more generations in the patchy than in a comparable homogeneous population, where 0 < FST < or = 0.25 is the fraction of genetic variance due to the sample of families across patches in one generation. In natural populations of Drosophila, therefore, the contribution of deleterious mutants to the genetic variance in fitness might be larger than previously thought. A model of density-dependent viability selection, inspired by the suggestion that deleterious effects can substantially increase when the environment becomes harsher, also gives credence to the analytical results and illustrates that mean persistence times are very sensitive to changes in ecological parameters. If the density dependence model can be taken seriously, there is a clear difficulty in comparing observed and expected levels of genetic variance on the basis of the simplest mutation-selection balance model.

Experimental evolution in Chlamydomonas II. Genetic variation in strongly contrasted environments

Experimental populations of Chlamydomonas were selected in Light (photoautotrophic) or Dark (heterotrophic) environments. Each population was a clone, founded by a single spore and propagated vegetatively thereafter. A heterogeneous environment was simulated by mixing Light and Dark lines in each growth cycle and redistributing them between the two environments in the next cycle. Some lines maintained permanently in the Dark evolved greatly increased growth within fewer than 300 generations, at the expense of reduced growth in the Light. Lines maintained in both Light and Dark environments evolved a negative genetic correlation between Light and Dark growth, and displayed more genetic variance of fitness than lines maintained in either environment exclusively. It is possible that genetic variance near mutation–selection balance is greater in heterogeneous environments because selection is weaker. However, the evolution of distinctly specialized lineages in these experiments suggests that in the conditions of batch culture a cost of adaptation creates negative frequency-dependent selection that maintains genetic variance. Genetic variance was greater in the more permissive environment (Light) than in the more restrictive environment (Dark).

Experimental evolution in Chlamydomonas. I. Short-term selection in uniform and diverse environments

Genetically diverse cultures of the unicellular chlorophyte Chlamydomonas were selected for about 50 generations in a heterogeneous environment, comprising eight different culture media, and in a uniform environment consisting of the average of the eight different media. The genetic variance of fitness, either across or within media, was reduced much more severely in the uniform than in the heterogeneous environment. This effect appears to have been caused by the obstruction of directional selection in the heterogeneous environment, leading to the retention of a greater quantity of genetic variance in the short term.

Estimation of deleterious-mutation parameters in natural populations.

The rate and average effects of spontaneous deleterious mutations are important determinants of the evolution of breeding systems and of the vulnerability of small populations to extinction. Nevertheless, few attempts have been made to estimate the properties of such mutations, and those studies that have been performed have been extremely labor intensive, relying on long-term, laboratory mutation-accumulation experiments. We present an alternative to the latter approach. For populations in which the genetic variance for fitness is a consequence of selection-mutation balance, the mean fitness and genetic variance of fitness in outbred generations can be expressed as simple functions of the genomic mutation rate, average homozygous effect and average dominance coefficient of new mutations. Using empirical estimates for the mean and genetic variance of fitness, these expressions can then be solved to obtain joint estimates of the deleterious-mutation parameters. We employ computer simulations to evaluate the degree of bias of the estimators and present some general recommendations on the application of the technique. Our procedures provide some hope for obtaining estimates of the properties of deleterious mutations from a wide phylogenetic range of species as well as a mechanism for testing the validity of alternative models for the maintenance of genetic variance for fitness.

ENVIRONMENT-DEPENDENCE OF QUANTITATIVE GENETIC PARAMETERS IN IMPATIENS PALLIDA.

Population response to selection depends on the presence of additive genetic variance for traits under selection. When a population enters an alien environment, environment-induced changes in the expression of genetic variance may occur. These could have large effects on the response to selection. To investigate the environment-dependence of genetic variance, we conducted a reciprocal transplant experiment between two ecotypically differentiated populations of Impatiens pallida using the progeny of a standard mating design. The floodplain site was characterized by high water availability, moderate temperatures, and continuous dense stands of Impatiens. The hillside site was drier, with larger temperature extremes and supported only scattered patches of Impatiens with significantly lower seed production and earlier mortality. Estimates of heritability were low for each of the 13 traits measured in each population and site (range from 0-28%). Additive genetic variance for life-history traits tended to be larger than for morphological traits, but genetic variance in fitness was estimated to be not significantly different from zero in all cases. Significant heritability was detected in both populations for one trait (date of first cleistogamous flower) known to be closely related to fitness on the hillside. In general, heritability was reduced for populations when grown in the hillside site relative to the floodplain site, suggesting that stress acts to reduce the expression of genetic variance and the potential to respond to selection there. Consistent reductions in heritability associated with more stressful environments suggest that populations invading such sites may undergo little adaptive differentiation and be more prone to local extinction.

INBREEDING: ITS EFFECT ON RESPONSE TO SELECTION FOR PUPAL WEIGHT AND THE HERITABLE VARIANCE IN FITNESS IN THE FLOUR BEETLE, TRIBOLIUM CASTANEUM.

We report our studies of the effect of inbreeding on the response to selection for increased pupal weight in the flour beetle, Tribolium castaneum. We also report the effects of inbreeding and selection for pupal weight on the heritable variation in fitness and fitness components. We created replicate and independent inbred lines with F-values of 0.00, 0.375, and 0.672, by 0, 2, and 5 generations, respectively, of brother-sister mating of adult beetles from an outbred stock population. Subsequently, we imposed artificial within-family selection for increased pupal weight in each of 15 inbred lines for eight generations; each line had its own paired, unselected control. We compared the response to selection across the three levels of inbreeding with theoretical expectation, and investigated the effects of inbreeding and selection on fitness variation among families within all 30 selected and control lines. Among-line variation in pupal weight increased with increased inbreeding prior to selection but diminished with directional selection. Inbreeding reduced the realized heritability of pupal weight concordant with quantitative predictions of additive theory. Mean fitness, measured in several ways, declined with inbreeding and declined further with selection. In contrast, the genetic variation for fitness in the inbred and selected lines lines equalled or exceeded that of the outbred controls. Our results suggest that inbreeding and selection may affect traits in different ways depending on the relative amounts of additive and nonadditive genetic variation.

Recombination load associated with selection for increased recombination.

Experiments on Drosophila suggest that genetic recombination may result in lowered fitness of progeny (a 'recombination load'). This has been interpreted as evidence either for a direct effect of recombination on fitness, or for the maintenance of linkage disequilibria by epistatic selection. Here we show that such a recombination load is to be expected even if selection favours increased genetic recombination. This is because of the fact that, although a modifier may suffer an immediate loss of fitness if it increases recombination, it eventually becomes associated with a higher additive genetic variance in fitness, which allows a faster response to direction selection. This argument applies to mutation-selection balance with synergistic epistasis, directional selection on quantitative traits, and ectopic exchange among transposable elements. Further experiments are needed to determine whether the selection against recombination due to the immediate load is outweighed by the increased additive variance in fitness produced by recombination.

Adaptive Topography in Fertility-Viability Selection Models: The Haplodiploid Case

A linear combination of partial changes of mean fitnesses from one generation to the next one is shown to be approximately equal to the additive genetic variance in fitness after enough generations and away from equilibrium in random mating haplodiploid populations under arbitrary weak frequency-dependent selection on sex-differentiated viability of individuals and sex-differentiated fertility of matings controlled at a single multiallelic locus. The result can be applied to X-linked locus models in diploid populations. The result is used to deduce approximate adaptive topographies far frequency-independent selection models in the cases of nonsex-differentiated fertilities and multiplicative sex-differentiated fertilities and for kin selection models in family-structured populations under the assumptions of single insemination and multiple insemination of females. Multiple insemination creates frequency-dependent selection regimes.

Pleiotropic models of polygenic variation, stabilizing selection, and epistasis.

We show that in polymorphic populations many polygenic traits pleiotropically related to fitness are expected to be under apparent "stabilizing selection" independently of the real selection acting on the population. This occurs, for example, if the genetic system is at a stable polymorphic equilibrium determined by selection and the nonadditive contributions of the loci to the trait value either are absent, or are random and independent of those to fitness. Stabilizing selection is also observed if the polygenic system is at an equilibrium determined by a balance between selection and mutation (or migration) when both additive and nonadditive contributions of the loci to the trait value are random and independent of those to fitness. We also compare different viability models that can maintain genetic variability at many loci with respect to their ability to account for the strong stabilizing selection on an additive trait. Let Vm be the genetic variance supplied by mutation (or migration) each generation, Vg be the genotypic variance maintained in the population, and n be the number of the loci influencing fitness. We demonstrate that in mutation (migration)-selection balance models the strength of apparent stabilizing selection is order Vm/Vg. In the overdominant model and in the symmetric viability model the strength of apparent stabilizing selection is approximately 1/(2n) that of total selection on the whole phenotype. We show that a selection system that involves pairwise additive by additive epistasis in maintaining variability can lead to a lower genetic load and genetic variance in fitness (approximately 1/(2n) times) than an equivalent selection system that involves overdominance. We show that, in the epistatic model, the apparent stabilizing selection on an additive trait can be as strong as the total selection on the whole phenotype.

THE INCREASED POTENTIAL FOR SELECTION OF THE LAC OPERON OF ESCHERICHIA COLI.

The fitness effects of six lac operons from natural isolates of Escherichia coli were determined in chemostats, in a test of the idea that selective differences among natural alleles are greater in novel conditions than in the prevailing environment, resulting in a greater genetic variance in fitness in novel conditions. Fitnesses were determined in the common milk sugar lactose, the natural substrate of the lac operon, and in three rare β-galactosides, lactulose, galactosyl-arabinose, and methyl-galactopyranoside, that are novel for E. coli. Significantly greater fitness differences were observed among the lac alleles in each of the novel β-galactosides than in lactose. An alternative explanation of the experimental findings is discussed. General evolutionary causes and consequences of selection potentials are discussed, and an outline of the work necessary to further elucidate the physiological basis of the observed potential for selection of the lac operon of E. coli is presented.

ON THE MAINTENANCE OF GENETIC VARIATION BY DISRUPTIVE SELECTION AMONG HOSTS IN A PHYTOPHAGOUS MITE

The phytophagous mite Tetranychus urticae is broadly polyphagous, having been reported from hundreds of different host species in many different families (Jeppson et al., 1975). Some hosts, such as varieties of tomato and cucumber, typically cause high juvenile mortality of T. urticae (e.g., Gould, 1978a, 1979; Fry, 1988a, 1989), even though these hosts are often used by natural populations of the mites (Gilbert et al., 1966; Gould, 1978b; Fry, 1988a). In laboratory experiments, however, T. urticae populations have been shown to be able to rapidly adapt to tomato, cucumber, and other initially unfavorable hosts, sometimes experiencing more than two-fold gains in survival in under 10 generations (Gould, 1979; Fry, 1989). This raises the question of how genetic variation for fitness on these hosts is maintained. In other words, why should populations often be far below their fitness maxima in environments they normally encounter? One obvious way of answering this question is to invoke trade-offs in adaptation to different hosts (Gould, 1979; Rausher, 1983; Mitter and Futuyma, 1983; Futuyma and Peterson, 1985). If genotypes favored by selection on some hosts are selected against on others, this could keep populations from attaining their fitness maximum on any host. In fact, experiments by Gould (1979) and Fry (1990) support the trade-off hypothesis for T. urticae. In these experiments, laboratory populations that had been allowed to adapt to cucumber and tomato, respectively, lost a considerable proportion of that adaptation after being maintained on a third host, lima bean, for about 10 generations. Selection rather than genetic drift appeared to be the more likely explanation for this reversion, because population sizes were on the order of 1,000 or more. While the reversion in the above experiments gave evidence that genotypes that were relatively well adapted to cucumber or tomato were selected against on bean, neither Gould nor Fry could detect statistically significant differences between the cucumber or tomato-adapted line and the control line in survival or fecundity on bean. In Fry's (1990) study, a confidence interval showed that fecundity on bean of the tomatoadapted line was probably not more than 10% lower than that of the control line. The fitness comparisons on bean in both studies were conducted under un-

Long-Term Experimental Evolution in Escherichia coli. I. Adaptation and Divergence During 2,000 Generations

We assess the degree to which adaptation to a uniform environment among independently evolving asexual populations is associated with increasing divergence of those populations. In addition, we are concerned with the pattern of adaptation itself, particularly whether the rate of increase in mean fitness tends to decline with the number of generations of selection in a constant environment. The correspondence between the rate of increase in mean fitness and the within-population genetic variance of fitness, as expected from Fisher's fundamental theorem, is also addressed. Twelve Escherichia coli populations were founded from a single clonal ancestor and allowed to evolve for 2,000 generations. Mean fitness increased by about 37%. However, the rate of increase in mean fitness was slower in later generations. There was no statistically significant within-population genetic variance of fitness, but there was significant between-population variance. Although the estimated genetic variation in fitness within populations was not statistically significant, it was consistent in magnitude with theoretical expectations. Similarly, the variance of mean fitness between populations was consistent with a model that incorporated stochastic variation in the timing and order of substitutions at a finite number of nonepistatic loci, coupled with substitutional delays and interference between substitutions arising from clonality. These results, taken as a whole, are consistent with theoretical expectations that do not invoke divergence due to multiple fitness peaks in a Wrightian evolutionary landscape.

GENETIC VARIANCE FOR RATE OF POPULATION INCREASE IN NATURAL POPULATIONS OF FLOUR BEETLES, TRIBOLIUM SPP.

The genetic and ecological effects of population subdividsion were investigated for two wild strains of Tribolium castaneum and two wild strains of T. confusum and compared with the effects of population subdivision on the synthetic laboratory strain of T. castaneum (c-SM), used extensively in earlier experiments. For the c-SM strain, it has been shown repeatedly, for a variety of different population structures (different combinations of effective numbers, Ne , and migration rates, m), that large heritable differences in population growth rate arise among demes during 10 to 15 generations of population subdivision. Because this laboratory strain was synthesized by mass mating several "inbred" strains in 1973 (80 to 100 generations ago), it is possible that it has genetic variation for fitness (measured as the heritable variance among demes in the rate of population increase) unusually large compared to natural populations of flour beetles. In this paper, I report that natural populations of flour beetle exhibit as much or more phenotypic and genetic variation in the effects of population structure on fitness than the laboratory strain, c-SM. The observation of substantial heritable variation for fitness in natural populations is unexpected under additive theory and may be indicative of nonadditive genetic variance.

CHAOBORUS PREDATION AND LIFE-HISTORY EVOLUTION IN DAPHNIA PULEX: TEMPORAL PATTERN OF POPULATION DIVERSITY, FITNESS, AND MEAN LIFE HISTORY.

The effect of predation by the aquatic dipteran larva Chaoborus americanus on genetic diversity and life-history evolution in the cladoceran Daphnia pulex was investigated in large replicate laboratory populations. Instantaneous daily loss rates of clonal diversity and genetic variance for fitness indicate that 93-99% of initial genetic diversity can be removed from populations during the 8-12 generations of clonal reproduction that occur each year in natural populations. In the absence of predation, the principal evolved changes in mean population life history were smaller immature body size and increased and earlier fecundity. In the presence of size-selective Chaoborus predation, populations evolved toward larger body size and increased and earlier reproduction. The difference between these two trajectories is an estimate of the direct additive effect of Chaoborus predation. This effect was manifested as evolution toward larger body size with a trend toward earlier and increased reproduction.

Evolutionary principles for polynomial models of frequency-dependent selection

A one-locus two-allele deterministic model of frequency-dependent selection is analyzed, where genotypic fitnesses [w(i)(q)] are assumed to be nth-degree polynomial functions of allelic frequency (q). The model encompasses many modes of selection, including intraspecies competitive interaction, brood selection, meiotic drive, cyclical selection, and mixed models. Allelic frequencies converge monotonically to locally stable equilibria provided that dw(i)(q)/dq is not large. There exists a function T(q) that is nondecreasing and locally maximized at locally stable equilibria. The rate of change of T(q) per generation is approximately equal to the additive genetic variance in fitness. T(q) is a simple function of the average effect of an allelic substitution and is closely related to Wright's "fitness function." These results define "evolutionary landscapes" for some complex selection processes and enlarge the scope of the classical methods embodied in Wright's "mean fitness principle" and Fisher's "fundamental theorem."

Relative fitness can decrease in evolving asexual populations of S. cerevisiae

It is generally accepted from the darwinian theory of evolution that a progressive increase in population adaptation will occur in populations containing genetic variation in fitness, until a stable equilibrium is reached and/or the additive genetic variation is exhausted. However, the theoretical literature of population genetics documents exceptions where mean population fitness may decrease in response to evolutionary changes in gene frequency, due to varying selective coefficients, sexual selection or to epistatic interactions between loci. Until now, no examples of such exceptions have been documented from fitness estimates in either natural or experimental populations. We present here direct evidence that, as a result of epistatic interactions between adaptive mutations, mean population fitness can decrease in asexual evolving populations of the yeast Saccharomyces cerevisiae.

AVERAGE FITNESS OF POPULATIONS OF DROSOPHILA MELANOGASTER AS ESTIMATED USING COMPOUND-AUTOSOME STRAINS.

The purpose of this paper and its companion (Hartl and Jungen, 1979) is to present a novel approach to obtaining an operational measure of average fitness in populations of Drosophila melanogaster. The procedure, which makes use of special strains carrying compound autosomes, yields a measure of population fitness that includes such components of fitness as mating speed, fertility, duration of fertile period, fecundity, egg hatchability, viability, efficiency of food assimilation, and growth rate, each component automatically given weight according to its actual importance under the experimental conditions. Furthermore, the procedure can be used to estimate average fitness of genetically heterogeneous populations, preserving intact whatever polymorphisms, epistasis, and linkage disequilibrium may be present in the original population. Because the average fitness of a population is frequently maximized by evolution in simple theoretical models of selection (Wright, 1937), and because in such models average fitness increases at a rate equal to the additive genetic variance in fitness (Fisher, 1930), the concept of average fitness of a population has played a key historical role in population genetics theory. (See Edwards, 197 7, for a review.) On the other hand, the average fitness of a population is not a readily estimated parameter. Total fitness can be split into its various components, to be sure, and these components can be estimated in individual genotypes, but the actual estimation of fitness components is a tricky business (Prout, 1971). Even so, experimental studies of fitness components have given rise to an enormous literature. (See Lewontin, 1974, and Wright, 1977, for reviews.) Attempting to translate fitness components as estimated in individual genotypes back into an estimate of population fitness runs up against two principal difficulties, however. First, estimation of fitness components does not resolve the question of which components are the key ones in terms of overall fitness; secondly, in estimating fitness components the genome must usually be studied chromosome by chromosome, as in the celebrated Curly-Plum method of viability estimation, and therefore any important nonrandom allelic or chromosomal associations that may exist are disrupted by the experimental procedure itself. Many of the practical problems encountered in trying to estimate average population fitness can be overcome by the use of so-called compound-autosome strains. Such strains have received considerable interest recently because of their potential practical utility in insect population control; compound-autosome strains can, in theory, be used to introduce conditional deleterious mutations into natural populations (Whitten, 1971; Foster et al., 1972). As a consequence, the behavior of compound-autosome strains in laboratory populations has been studied extensively I Supported by NSF grant PCM77-00886. D. L. H. is recipient of Research Career Award GM0002301. This paper is dedicated to the memory of Spencer W. Brown.