The alignment between phenotypic plasticity,the major axis of genetic variation and the response to selection

Phenotypic plasticity is the ability of a genotype to produce more than one phenotype in order to match the environment. Recent theory proposes that the major axis of genetic variation in a phenotypically plastic population can align with the direction of selection. Therefore, theory predicts that plasticity directly aids adaptation by increasing genetic variation in the direction favoured by selection and reflected in plasticity. We evaluated this theory in the freshwater crustacean Daphnia pulex, facing predation risk from two contrasting size-selective predators. We estimated plasticity in several life-history traits, the G matrix of these traits, the selection gradients on reproduction and survival, and the predicted responses to selection. Using these data, we tested whether the genetic lines of least resistance and the predicted response to selection aligned with plasticity. We found predator environment-specific G matrices, but shared genetic architecture across environments resulted in more constraint in the G matrix than in the plasticity of the traits, sometimes preventing alignment of the two. However, as the importance of survival selection increased, the difference between environments in their predicted response to selection increased and resulted in closer alignment between the plasticity and the predicted selection response. Therefore, plasticity may indeed aid adaptation to new environments.     

Selection response and efficiency of doubled-haploid recurrent selection in a cross-fertilized species

Summary Computer simulation was used to compare the simulated response to doubled-haploid (DH) mass selection with the response predicted by mathematical formulae. The efficiency of DH versus diploid mass selection in a cross-fertilized species was also studied by means of theoretical consideration and computer simulation. Simulated gain was in agreement with the predicted gain in the DH population under both additive and complete dominance models. The simulated variance of response to DH mass selection was close to the predicted variance at both the 5% and 25% selection regimes under additive and complete dominance models. The efficiency of DH over diploid mass selection was shown to be dependent upon the allelic frequency, the degree of dominance, and the amount of environmental variance. In theory the efficiency can range from zero to infinity, but in reality it should be greater than one. The efficiency ranges from 2 to 2 in the absence of dominance; it can be greater than two only in the presence of dominance and a small environmental variance. The variance of response to DH mass selection can be smaller than or up to twice as large as the variance of response to diploid mass selection. Computer simulation results agreed with the predicted efficiency of DH mass selection and with the predicted variance-of-response ratio of DH mass selection to diploid mass selection.Joint Contribution from the Charlottetown Research Station, contribution no. 604 and Department of Crop Science, University of Guelph     

Predicting the evolution of sexual size dimorphism

11 , Evolution 34 : 292–305) equations for predicting the evolution of sexual size dimorphism (SSD) through frequency‐dependent sexual selection, and frequency‐independent natural selection, were tested against results obtained from a stochastic genetic simulation model. The SSD evolved faster than predicted, due to temporary increases in the genetic variance brought about by directional selection. Predictions for the magnitude of SSD at equilibrium were very accurate for weak sexual selection. With stronger sexual selection the total response was greater than predicted. Large changes in SSD can occur without significant long‐term change in the genetic correlation between the sexes. Our results suggest that genetic correlations constrain both the short‐term and long‐term evolution of SSD less than predicted by the Lande model.     

More on the efficiency of marker-assisted selection

 Computer simulations were used to study the efficiency of marker-assisted selection (MAS) based on an index combining the phenotypic value and the molecular score of individuals. The molecular score is computed from the effects attributed to markers by multiple regression of phenotype on marker genotype. The results show that in the first generation the ratio RE of the expected efficiency of MAS over the expected efficiency of purely phenotypic selection generally increases when considering: (1) larger population sizes, (2) lower heritability values of the trait, and (3) a higher type-I error risk of the regression. This is consistent with previously published results. However, at low heritabilities our results point out that response to MAS is more variable than response to phenotypic selection. Hence, when the difference of genetic gains is considered instead of their ratio, RE, the heritability values corresponding to maximal advantage of using MAS rather than phenotypic selection are still low, but higher than predicted based on RE. The study over several successive generations of the rate of fixation of QTLs shows that the higher efficiency of MAS on QTLs with large effects in early generations is balanced by a higher rate of fixation of unfavourable alleles at QTLs with small effects in later generations. This explains why MAS may become less efficient than phenotypic selection in the long term. MAS efficiency therefore depends on the genetic determinism of the trait. Finally, we investigate a modified MAS method involving an alternation of selection on markers with and without phenotypic evaluation. Our results indicate that such a selection method could at low cost, provide an important increase in the genetic gain per unit of time in practical breeding programs. Received: 11 July 1997 / Accepted: 4 August 1997     

Artificial selection on larval growth curves in Tribolium: correlated responses and constraints

Body size is often constrained from evolving. Although artificial selection on body size in insects frequently results in a sizable response, these responses usually bear fitness costs. Further, these experiments tend to select only on size at one landmark age, rather than selecting for patterns of growth over the whole larval life stage. To address whether constraints may be caused by larval growth patterns rather than final size, we implemented a function‐valued (FV) trait method of selection, in which entire larval growth curves from Tribolium were artificially selected. The selection gradient function used was previously predicted to give the maximal response and was implemented using a novel selection index in the FV framework. Results indicated a significant response after one generation of selection, but no response in subsequent generations. Correlated responses included increased mortality, increased critical weight, and decreased development time (DT). The lack of response in size and development time after the first generation was likely caused by increased mortality suffered in selected lines; we demonstrated that the selection criterion caused both increased body size and increased mortality. We conclude that artificial selection on continuous traits using FV methods is very efficient and that the constraint of body size evolution is likely caused by a suite of trade‐offs with other traits.     

SEXUAL SIZE DIMORPHISM AS A CORRELATED RESPONSE TO SELECTION ON BODY SIZE: AN EMPIRICAL TEST OF THE QUANTITATIVE GENETIC MODEL

We artificially selected for body size in Drosophila melanogaster to test Lande's quantitative genetic model for the evolution of sexual size dimorphism. Thorax width was used as an estimator of body size. Selection was maintained for 21 generations in both directions on males only, females only, or both sexes simultaneously. The correlated response of sexual size dimorphism in each selection regime was compared to the response predicted by four variants of the model, each of which differed only in assumptions about input parameters. Body size responded well to selection, but the correlated response of sexual size dimorphism was weaker than that predicted by any of the variants. Dimorphism decreased in most selection lines, contrary to the model predictions. We suggest that selection on body size acts primarily on growth trajectories. Changes in dimorphism are caused by the fact that male and female growth trajectories are not parallel and termination of growth at different points along the curves results in dimorphism levels that are difficult to predict without detailed knowledge of growth parameters. This may also explain many of the inconsistent results in dimorphism changes seen in earlier selection experiments.     

A Population Genetics Model of Marker-Assisted Selection

A deterministic two-loci model was developed to predict genetic response to marker-assisted selection (MAS) in one generation and in multiple generations. Formulas were derived to relate linkage disequilibrium in a population to the proportion of additive genetic variance used by MAS, and in turn to an extra improvement in genetic response over phenotypic selection. Predictions of the response were compared to those predicted by using an infinite-loci model and the factors affecting efficiency of MAS were examined. Theoretical analyses of the present study revealed the nonlinearity between the selection intensity and genetic response in MAS. In addition to the heritability of the trait and the proportion of the marker-associated genetic variance, the frequencies of the selectively favorable alleles at the two loci, one marker and one quantitative trait locus, were found to play an important role in determining both the short- and long-term efficiencies of MAS. The evolution of linkage disequilibrium and thus the genetic response over several generations were predicted theoretically and examined by simulation. MAS dissipated the disequilibrium more quickly than drift alone. In some cases studied, the rate of dissipation was as large as that to be expected in the circumstance where the true recombination fraction was increased by three times and selection was absent.     

Potential for improvement by selection for reducing sugar content after cold storage for three potato populations

The objectives of this study were to examine the expected response to selection for reducing-sugar content after cold storage in three hybrid populations, to determine whether these populations included clones low in reducing sugars, and to investigate the effectiveness of indirect selection for chip colour based on selection of sugar content after cold storage. The three hybrid populations included: a random sample of 39 clones of Population 1, which was derived from crossing ND860-2 (a clone low in reducing sugars) with F58089 (a clone intermediate in reducing sugars); 40 clones of Population 2, which was obtained from crossing ND860-2 with Russette (a clone high in reducing sugars); and 40 clones of Population 3, which was derived from crossing Russette with F58089. Sugar content and chip colour were assessed in tubers stored for 2 months at 4 °C at Cambridge, Ontario, and at 3 °C at Benton Ridge, New Brunswick. Population 1 had a slightly greater predicted response to selection for reduction in glucose and total reducing sugars than the other two populations. This could be attributed to higher heritability estimates for Population 1, which was a reflection of smaller clone × environment interaction mean squares. The greater potential advance by selection for fructose, glucose, and total reducing sugars, was a direct consequence of its lower means for these traits. Low reducing-sugar clones were found in all three populations, indicating their potential use for the selection of low reducing sugars. Populations 2 and 3, however, would require stronger selection pressures and, therefore, large population sizes. Expected correlated responses for chip colour by selection for fructose and glucose were similar to, and sometimes exceeded, the expected direct responses in all three populations. Indirect responses for chip colour by selection for sucrose, however, were lower than direct selection responses. These results indicate that indirect selection for chip colour, by selection for either fructose or glucose content after cold storage, is as effective as direct selection for chip colour.     

Human testis-specific genes are under relaxed negative selection

Recent studies have suggested that selective forces and constraints acting on genes varied during human evolution depending on the organ in which they are expressed. To gain insight into the evolution of organ determined negative selection forces, we compared the non-synonymous SNP diversity of genes expressed in different organs. Based on a HAPMAP dataset, we determined for each SNP its frequency in 11 human populations and, in each case, predicted whether or not the change it produces is deleterious. We have shown that, for all organs under study, SNPs predicted to be deleterious are present at a significantly lower frequency than SNPs predicted to be tolerated. However, testis-specific genes contain a higher proportion of deleterious SNPs than other organs. This study shows that negative selection is acting on the whole human genome, but that the action of negative selection is relaxed on testis-specific genes. This result adds to and expands the hypothesis of a recent evolutionary change in the human male reproductive system and its behavior.     

Multilevel selection 2: Estimating the genetic parameters determining inheritance and response to selection

Interactions among individuals are universal, both in animals and in plants and in natural as well as domestic populations. Understanding the consequences of these interactions for the evolution of populations by either natural or artificial selection requires knowledge of the heritable components underlying them. Here we present statistical methodology to estimate the genetic parameters determining response to multilevel selection of traits affected by interactions among individuals in general populations. We apply these methods to obtain estimates of genetic parameters for survival days in a population of layer chickens with high mortality due to pecking behavior. We find that heritable variation is threefold greater than that obtained from classical analyses, meaning that two-thirds of the full heritable variation is hidden to classical analysis due to social interactions. As a consequence, predicted responses to multilevel selection applied to this population are threefold greater than classical predictions. This work, combined with the quantitative genetic theory for response to multilevel selection presented in an accompanying article in this issue, enables the design of selection programs to effectively reduce competitive interactions in livestock and plants and the prediction of the effects of social interactions on evolution in natural populations undergoing multilevel selection.     

Predictions of patterns of response to artificial selection in lines derived from natural populations

The pattern of response to artificial selection on quantitative traits in laboratory populations can tell us something of the genetic architecture in the natural population from which they were derived. We modeled artificial selection in samples drawn from natural populations in which variation had been maintained by recurrent mutation, with genes having an effect on the trait, which was subject to real stabilizing selection, and a pleitropic effect on fitness (the joint-effect model). Natural selection leads to an inverse correlation between effects and frequencies of genes, such that the frequency distribution of genes increasing the trait has an extreme U-shape. In contrast to the classical infinitesimal model, an early accelerated response and a larger variance of response among replicates were predicted. However, these are reduced if the base population has been maintained in the laboratory for some generations by random sampling prior to artificial selection. When multiple loci and linkage are also taken into account, the gametic disequilibria generated by the Bulmer and Hill-Robertson effects are such that little or no increase in variance and acceleration of response in early generations of artificial selection are predicted; further, the patterns of predicted responses for the joint-effect model now become close to those of the infinitesimal model. Comparison with data from laboratory selection experiments shows that, overall, the analysis did not provide clear support for the joint-effect model or a clear case for rejection.     

Selection indices for non-linear profit functions

Summary Conventional selection index theory assumes that the total merit or profitability of animals is a linear function of measurable traits. However, in many cases merit may be a non-linear function of these traits. A linear selection index can still be used in this situation but the optimum index depends on the selection intensity to be used and on the number of generation over which the selection response is to be maximized. Nonlinear selection indices have been suggested but these result in a lower selection response than the best linear index. Linear selection indices suggested in the past are shown to correspond to the optimum linear index for either a very small selection response or, in the case of restricted indices, a very large selection response. The economic value of a trait may depend on management decisions taken by the farmer. In this situation the economic values should be calculated assuming that the management decisions taken maximize profit given the present genetic value of the animals.     

An experimental test of the efficiency of family selection in chickens

Summary Responses to single trait selection on individual phenotype and sire-family mean phenotype for survivor's egg weight and rate of lay were measured for a single generation in 13 replicates. Each replicate-selection criterion-trait subclass consisted of eight sire families or 72 females measured and was reproduced from the best 25% of the families or individuals. The realized heritability of egg weight was 0.39 and that of rate of lay was 0.31, both of which were significantly greater than zero but not significantly different from the predicted values based on halfsib correlations in the base population.The standardized response to sire-family selection was less than the response to individual selection for both traits and the difference was significant for rate of lay (0.10; 0.31) but not for egg weight (0.22; 0.39). The predicted responses to sire-family selection were less than those for individual selection for both traits, and the observed responses to sire-family selection were not significantly different from the predicted values for either trait.These experimental results do not disagree with the theoretical expectations of the relative efficiencies of individual and sire-family selection.Journal paper no. 7479, Purdue University, Agricultural Experiment Station. This investigation was conducted as a part of the cooperative research of the NC-89 Regional Poultry Breeding Project entitled Nature and Utilization of Genetic Variation in Poultry Improvement     

Selection with Partial Selfing. I. Mass Selection

The expected responses to mass selection carried out before or after reproduction in a population whose members all have a fixed probability of self pollination (s) are formulated using covariances of relatives and their component quadratic functions for a model with arbitrary additive and dominance effects. The response measured in the first generation offspring after selection (immediate gain) can differ from that retained when the population has regained equilibrium (permanent gain). The population mean behaves in a predictable manner during the return to equilibrium, and its value at any time can be predicted from earlier generations. The permanent gain from selection after reproduction is always (1 + s)/2 times as large as that from selection before reproduction, but the relationship of the immediate gains depends on the genetic model assumed. Numerical analysis applied to a model with two alleles per locus and varying allele frequencies, dominance ratios and numbers of loci showed that the proportion of the immediate gain retained at equilibrium was reduced with the large inbreeding depression associated with increasing dominance levels and numbers of loci and was generally lower for selection after reproduction than before. In the absence of information as to the magnitude of genetic variances and inbreeding depression in species reproducing by partial selfing, the importance of this phenomenon is unknown.     

Aging asexual lineages and the evolutionary maintenance of sex

Finite populations of asexual and highly selfing species suffer from a reduced efficacy of selection. Such populations are thought to decline in fitness over time due to accumulating slightly deleterious mutations or failing to adapt to changing conditions. These within‐population processes that lead nonrecombining species to extinction may help maintain sex and outcrossing through species level selection. Although inefficient selection is proposed to elevate extinction rates over time, previous models of species selection for sex assumed constant diversification rates. For sex to persist, classic models require that asexual species diversify at rates lower than sexual species; the validity of this requirement is questionable, both conceptually and empirically. We extend past models by allowing asexual lineages to decline in diversification rates as they age, that is nonrecombining lineages “senesce” in diversification rates. At equilibrium, senescing diversification rates maintain sex even when asexual lineages, at young ages, diversify faster than their sexual progenitors. In such cases, the age distribution of asexual lineages contains a peak at intermediate values rather than showing the exponential decline predicted by the classic model. Coexistence requires only that the average rate of diversification in asexuals be lower than that of sexuals.     

How closely does genetic diversity in finite populations conform to predictions of neutral theory? Large deficits in regions of low recombination

Levels of genetic diversity in finite populations are crucial in conservation and evolutionary biology. Genetic diversity is required for populations to evolve and its loss is related to inbreeding in random mating populations, and thus to reduced population fitness and increased extinction risk. Neutral theory is widely used to predict levels of genetic diversity. I review levels of genetic diversity in finite populations in relation to predictions of neutral theory. Positive associations between genetic diversity and population size, as predicted by neutral theory, are observed for microsatellites, allozymes, quantitative genetic variation and usually for mitochondrial DNA (mtDNA). However, there are frequently significant deviations from neutral theory owing to indirect selection at linked loci caused by balancing selection, selective sweeps and background selection. Substantially lower genetic diversity than predicted under neutrality was found for chromosomes with low recombination rates and high linkage disequilibrium (compared with 'normally' recombining chromosomes within species and adjusted for different copy numbers and mutation rates), including W (median 100% lower) and Y (89% lower) chromosomes, dot fourth chromosomes in Drosophila (94% lower) and mtDNA (67% lower). Further, microsatellite genetic and allelic diversity were lost at 12 and 33% faster rates than expected in populations adapting to captivity, owing to widespread selective sweeps. Overall, neither neutral theory nor most versions of the genetic draft hypothesis are compatible with all empirical results.     

Simultaneous selection on two fitness-related traits in the butterfly Bicyclus anynana

Abstract. Theory about the role of constraints in evolution is abundant, but few empirical data exist to describe the consequences a bias in phenotypic variation has for micro evolution. Responses to natural selection can be severely hampered by a genetic correlation among a suite of traits. Constraints can be studied using antagonistic selection experiments, that is, two-trait selection in opposition to this correlation. The two traits studied here were development time and wing pattern (eyespot size) in the butterfly Bicyclus anynana , both of which have a clear adaptive significance. Rates of response were higher for eyespot size than for development time, but were independent of the concurrent selection (either in the same direction as the correlation or perpendicular to it). Regimes differed in both traits in all directions after 11 generations of selection. The uncoupling lines had higher relative responses than the synergistic lines in development time and equal relative responses in eyespot size. The patterns for eyespot size (reaction norms) were consistent across different rearing temperatures. Differences in lines selected for fast and slow development time were more pronounced at lower temperatures, irrespective of the direction of joint wing pattern selection. Furthermore, correlated responses in pupal weight and growth rate were observed; lines selected for a slower development had higher pupal weights, especially at lower temperatures. The response of the uncoupling lines was not hampered by a lack of selectable genetic variation, and the relative response in the development time was larger than expected based on response in the coupled direction and quantitative genetic predictions. This suggests that the structure of the genetic architecture does not constrain the short-term, independent evolution of both wing pattern and development time.     

Modes of selection and recombination response in Drosophila melanogaster

A selection experiment for sternopleural bristle number in Drosophila melanogaster was undertaken to analyze the correlated effects on recombination. Replicate lines were subjected to divergent directional selection and to stabilizing selection. Recombination rates for markers on chromosomes 2 (dp-cn-bw) and 3 (se-ss-ro) were compared to those from a control. All lines responded as predicted for bristle number. Lines selected for both increased and decreased bristle number exhibited significantly increased recombination rates. The predicted recombination response from stabilizing selection is suggested by our data, but only one comparison is statistically significant. These results, taken with other studies, support the proposal that genetic recombination enhances individual fitness when populations are experiencing environmental change. Less conclusively, our results suggest that populations undergoing stabilizing selection may respond by reducing their rates of crossing over.     

The influence of aberrant values on the statistics related to a selection program

Summary Examples are presented to illustrate some of the effects aberrant values, in particular, measurement errors, may have on estimates of the genetic parameters related to selection studies. It is shown that aberrant values may cause observed response to selection pressure to differ considerably from predicted response. Possible dangers of indiscriminate screening are also discussed.     

An exact form of the breeder's equation for the evolution of a quantitative trait under natural selection

Starting with the Price equation, I show that the total evolutionary change in mean phenotype that occurs in the presence of fitness variation can be partitioned exactly into five components representing logically distinct processes. One component is the linear response to selection, as represented by the breeder's equation of quantitative genetics, but with heritability defined as the linear regression coefficient of mean offspring phenotype on parent phenotype. The other components are identified as constitutive transmission bias, two types of induced transmission bias, and a spurious response to selection caused by a covariance between parental fitness and offspring phenotype that cannot be predicted from parental phenotypes. The partitioning can be accomplished in two ways, one with heritability measured before (in the absence of) selection, and the other with heritability measured after (in the presence of) selection. Measuring heritability after selection, though unconventional, yields a representation for the linear response to selection that is most consistent with Darwinian evolution by natural selection because the response to selection is determined by the reproductive features of the selected group, not of the parent population as a whole. The analysis of an explicitly Mendelian model shows that the relative contributions of the five terms to the total evolutionary change depends on the level of organization (gene, individual, or mated pair) at which the parent population is divided into phenotypes, with each frame of reference providing unique insight. It is shown that all five components of phenotypic evolution will generally have nonzero values as a result of various combinations of the normal features of Mendelian populations, including biparental sex, allelic dominance, inbreeding, epistasis, linkage disequilibrium, and environmental covariances between traits. Additive genetic variance can be a poor predictor of the adaptive response to selection in these models. The narrow-sense heritability sigma2A/sigma2P should be viewed as an approximation to the offspring-parent linear regression rather than the other way around.