Additive Genetic Variance In Fitness Research Articles

Evolutionary genetics of ageing in the wild: empirical patterns and future perspectives

Summary 1 Classical evolutionary theory states that senescence should arise as a consequence of the declining force of selection late in life. Although the quantitative genetic predictions of hypotheses derived from this theory have been extensively tested in laboratory studies of invertebrate systems, relatively little is known about the genetics of ageing in the wild. 2 Data from long-term ecological studies is increasingly allowing quantitative genetic approaches to be used in studies of senescence in free-living populations of vertebrates. We review work to date and argue that the patterns are broadly consistent with theoretical predictions, although there is also a clear need for more empirical work. 3 We argue that further advances in this field of research might be facilitated by increased use of reaction norm models, and a decreased emphasis on attempting to discriminate between mutation accumulation and antagonistic pleiotropy models of senescence. We also suggest a framework for the better integration of environmental and genetic effects on ageing. 4 Finally, we discuss some of the difficulties in applying quantitative genetic models to studies of senescence outside the laboratory. In particular we highlight the problems that viability selection can cause for an accurate estimation of parameters used in the prediction of age-trajectory evolution.

FITNESS EFFECTS OF MUTATION ACCUMULATION IN A NATURAL OUTBRED POPULATION OF WILD RADISH (RAPHANUS RAPHANISTRUM): COMPARISON OF FIELD AND GREENHOUSE ENVIRONMENTS

Spontaneous deleterious mutation has been measured in a handful of organisms, always under laboratory conditions and usually employing inbred species or genotypes. We report the results of a mutation accumulation experiment with an outbred annual plant, Raphanus raphanistrum, with lifetime fitness measured in both the field and the greenhouse. This is the first study to report the effects of spontaneous mutation measured under field conditions. Two large replicate populations (N(e) approximately 600) were maintained with random mating in the greenhouse under relaxed selection for nine generations before the field assay was performed and ten generations before the greenhouse assay. Each generation, every individual was mated twice, once as a pollen donor and once as a pollen recipient, and a single seed from each plant was chosen randomly to create the next generation. The ancestral population was maintained as seeds at 4 degrees C. Declines in lifetime fitness were observed in both the field (1.7% per generation; P= 0.27) and the greenhouse (0.6% per generation; P= 0.07). Significant increases in additive genetic variance for fitness were found for stems per day, flowers per stem, fruits per flower and seeds per fruit in the field as well as for fruits per flower in the greenhouse. Lack of significance of the fitness decline may be due to the short period of mutation accumulation, the use of outbred populations, or both. The percent declines in fitness are at the high end of the range observed in other mutation accumulation experiments and give some support to the idea that mutational effects may be magnified under harsher field conditions. Thus, measurement of mutational parameters under laboratory conditions may underestimate the effects of mutations in natural populations.

Evidence for a Genetic Basis of Aging in Two Wild Vertebrate Populations

Aging, or senescence, defined as a decline in physiological function with age, has long been a focus of research interest for evolutionary biologists. How has natural selection failed to remove genetic effects responsible for such reduced fitness among older individuals? Current evolutionary theory explains this phenomenon by showing that, as a result of the risk of death from environmental causes that individuals experience, the force of selection inevitably weakens with age. This in turn means that genetic mutations having detrimental effects that are only felt late in life might persist in a population. Although widely accepted, this theory rests on the assumption that there is genetic variation for aging in natural systems, or (equivalently), that genotype-by-age interactions (GxA) occur for fitness. To date, empirical support for this assumption has come almost entirely from laboratory studies on invertebrate systems, most notably Drosophila and C. elegans, whereas tests of genetic variation for aging are largely lacking from natural populations. By using data from two wild mammal populations, we perform quantitative genetic analyses of fitness and provide the first evidence for a genetic basis of senescence to come from a study in the natural environment. We find evidence that genetic differences among individuals cause variation in their rates of aging and that additive genetic variance for fitness increases with age, as predicted by the evolutionary theory of senescence.

PERSPECTIVE: SIGN EPISTASIS AND GENETIC COSTRAINT ON EVOLUTIONARY TRAJECTORIES

Abstract Epistasis for fitness means that the selective effect of a mutation is conditional on the genetic background in which it appears. Although epistasis is widely observed in nature, our understanding of its consequences for evolution by natural selection remains incomplete. In particular, much attention focuses only on its influence on the instantaneous rate of changes in frequency of selected alleles via epistatic contribution to the additive genetic variance for fitness. Thus, in this framework epistasis only has evolutionary importance if the interacting loci are simultaneously segregating in the population. However, the selective accessibility of mutational trajectories to high fitness genotypes may depend on the genetic background in which novel mutations appear, and this effect is independent of population polymorphism at other loci. Here we explore this second influence of epistasis on evolution by natural selection. We show that it is the consequence of a particular form of epistasis, which we designate sign epistasis. Sign epistasis means that the sign of the fitness effect of a mutation is under epistatic control; thus, such a mutation is beneficial on some genetic backgrounds and deleterious on others. Recent experimental innovations in microbial systems now permit assessment of the fitness effects of individual mutations on multiple genetic backgrounds. We review this literature and identify many examples of sign epistasis, and we suggest that the implications of these results may generalize to other organisms. These theoretical and empirical considerations imply that strong genetic constraint on the selective accessibility of trajectories to high fitness genotypes may exist and suggest specific areas of investigation for future research.

PERSPECTIVE:SIGN EPISTASIS AND GENETIC CONSTRAINT ON EVOLUTIONARY TRAJECTORIES

Epistasis for fitness means that the selective effect of a mutation is conditional on the genetic background in which it appears. Although epistasis is widely observed in nature, our understanding of its consequences for evolution by natural selection remains incomplete. In particular, much attention focuses only on its influence on the instantaneous rate of changes in frequency of selected alleles via epistatic contribution to the additive genetic variance for fitness. Thus, in this framework epistasis only has evolutionary importance if the interacting loci are simultaneously segregating in the population. However, the selective accessibility of mutational trajectories to high fitness genotypes may depend on the genetic background in which novel mutations appear, and this effect is independent of population polymorphism at other loci. Here we explore this second influence of epistasis on evolution by natural selection. We show that it is the consequence of a particular form of epistasis, which we designate sign epistasis. Sign epistasis means that the sign of the fitness effect of a mutation is under epistatic control; thus, such a mutation is beneficial on some genetic backgrounds and deleterious on others. Recent experimental innovations in microbial systems now permit assessment of the fitness effects of individual mutations on multiple genetic backgrounds. We review this literature and identify many examples of sign epistasis, and we suggest that the implications of these results may generalize to other organisms. These theoretical and empirical considerations imply that strong genetic constraint on the selective accessibility of trajectories to high fitness genotypes may exist and suggest specific areas of investigation for future research.

The Fundamental Theorem of Natural Selection

R. A. Fisher's Fundamental Theorem of Natural Selection states that the rate of increase in the mean fitness of a population ascribable to gene-frequency changes is exactly equal to the additive genetic variance in fitness. It has been widely misunderstood, though clarification has gradually come about particularly through the work of G. R. Price, W. J. Ewens, and S. Lessard. Building on their interpretations we here explain the approach adopted by Fisher (1941), devising a figure as an aid to understanding this important paper.

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

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.

Fundamental theorem of natural selection in biocultural populations

I derive a general equation for the evolution of mean biological fitness in large, randomly mating populations in which the phenotype is subject to both biological and cultural transmission and in which fitness and the effects of cultural transmission are genotype-dependent. The equation is f m ̄ dt = 2 Cov(m, m′), where d m ̄ dt is the instantaneous rate of change in the mean biological fitness of the population and Cov( m, m′) is the covariance between offspring and parental fitnesses. This formulation differs from Fisher's fundamental theorem in at least two important respects. First, because covariances can be either positive or negative, mean fitness can decline over evolutionary time, in contrast to Fisher's result that fitness always increases. Second, since Cov( m, m′) is a phenotypic rather than a genotypic covariance, natural selection can bring about changes in mean fitness even in the absence of additive genetic variance for fitness. Comparison of simple models of vertical (from parents to offspring) and oblique (from members of the parental generation to offspring) cultural transmission indicates that in the former case, mean fitness can evolve in the absence of genotypic variation for both fitness and the effects of cultural transmission, while in the latter case, both are required for evolution to occur.

Quantitative Genetics in Natural Plant Populations: A Review of the Theory

The methods of quantitative genetics may be useful for quantifying constraints on the rate and direction of response to selection in natural plant populations. We review the assumptions necessary for accurate estimation and significance testing of quantitative-genetic parameters, and consider when such estimates may accurately predict a response to selection. Estimates of heritabilities and genetic correlations can provide good predictions of a long-term response to selection if (1) such estimates are reasonably accurate; (2) many genes contribute to genetic variances and covariances; (3) genetic variance-covariance matrices remain approximately constant through time (when major genes are important sources of variation, when selection is strong, or when populations are small, then rapid alterations in gene frequencies may occur, with consequent changes in the quantitative-genetic parameters); (4) genotype-environment interaction does not alter genetic parameters in new or unmeasured environments; and (5) populations are not inbred. The importance of these assumptions depends on the evolutionary scale of the questions we wish to ask. We discuss evolutionary interpretations of heritabilities and genetic correlations, emphasizing that the plasticity of quantitative-genetic parameters and the imprecision of their estimates are serious problems in the study of natural plant populations. It is important to separate the fundamental, long-term genetic constraints, which limit species evolution, from the transient genetic correlations that may be found in a particular population. It is unclear whether natural populations ever reach equilibrium conditions, in which the additive genetic variance for fitness is depleted. Under many circumstances it is difficult to deduce the past history of selection from the genetic architecture of metrical traits.

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."

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.

A Fundamental Theorem of Natural Selection for Sex Linkage or Arrhenotoky

Equation (11) is a general equation for the change in geometric mean fitness at a male haploid or sex-linked locus when the selection intensity is small. The rate of change in fitness depends on the additive genetic variance in fitness, which is defined as the variance of the additive genotypic values when the additive model of gene action assumes no dominance in females and complete dosage compensation in males. If the relative fitnesses of genotypes are constant, then under slow selection the increment in fitness is equal to the additive variance if either (1) the population is in random mating or (2) there is no dominance in females and complete dosage compensation in males. If both conditions hold, then a male haploid population evolves one-third faster than the corresponding diploid population and one-third slower than the corresponding haploid population. In computer-simulated populations undergoing random mating, the additive variance is a good approximation to actual fitness changes over a wide ra...

Some Aspects of Natural Selection in Arrhenotokous Populations

SYNOPSIS. Obligate arrhenotoky is known to have evolved only eight times, once each in the rotifer order Monogonanta, the arachnid order Acarina, the insect orders Hymenoptera and Thysanoptera, and in two families of Homoptera (Coccidae and Aleyrodidae) and Coleoptera (Scolytidae and Micromalthidae). In this paper it is argued that in male haploids the population genetic parameter which is most nearly analogous to the average fitness in ordinary diploids is the geometric mean of the average fitness in the two sexes. The geometric mean fitness is maximized by selection in a random mating population, provided one takes into account the fact that the system of inheritance imposes constraints on the gene frequencies in males and females. Furthermore, under sufficiently small selection intensities, the rate of change in geometric mean fitness is approximately equal to the additive genetic variance infitness, where the additive variance is defined as the variance due to the regression on a model of gene action which assumes no dominance in females and complete dosage compensation in males. Some problems concerning the sex ratio in male haploids when there is extreme inbreeding are also discussed.