Decay of unused characters by selection and drift

The reduction and loss of redundant phenotypic characters is a common feature of evolution. However, the mechanisms that drive deterioration of unused characters remain unclear. Here, we outline a simple framework where the relative importance of selective and neutral processes varies with environmental factors, because of variation in the fitness costs associated with unused traits. We tested our hypotheses using experimental evolution of the bacterium Pseudomonas fluorescens in spatially uniform environments. Results show that an unused character, swimming motility, decayed over evolutionary time and the rate of this decay varied among selection environments with different levels of resource availability. This is explained in the context of an environment-specific genetic correlation between motility and fitness, which is negative when resources are limited but neutral at higher resource levels. Thus, selection against an unused character was most effective in environments where the fitness cost was the greatest. This suggests that the same character can decay by different mechanisms depending upon environmental factors and supports previous evidence to show that resource availability can critically affect the outcomes of evolution.     

Phenotypic integration may constrain phenotypic plasticity in plants

Phenotypic plasticity is essential for plant adaptation to changing environments but some factors limit its expression, causing plants to fail in producing the best phenotype for a given environment. Phenotypic integration refers to the pattern and magnitude of character correlations and it might play a role as an internal constraint to phenotypic plasticity. We tested the hypothesis that phenotypic integration – estimated as the number of significant phenotypic correlations between traits – constrains phenotypic plasticity of plants. The rationale is that, for any phenotypic trait, the more linked with other traits it is, the more limited is its range of variation. In the perennial species Convolvulus chilensis (Convolvulaceae) and Lippia alba (Verbenaceae) we determined the relationship between phenotypic plasticity to relevant environmental factors – shading for C. chilensis and drought for L. alba– and the magnitude of phenotypic integration of morphological and biomass allocation traits. In C. chilensis plants, plasticity to shading of a given trait decreased with the number of significant correlations that it had with the other traits. Likewise, the characters that showed greater plasticity to experimental drought in L. alba plants had fewer significant phenotypic correlations with other characters. We report a novel limit to phenotypic plasticity of plants by showing that the phenotypic trait architecture may constrain their plastic, functional responses to the environment.     

Estimates of Stability Parameters in Dioscorea deltoidea Wall

Estimates of stability parameters for various traits in Dioscoreadeltoidea revealed that some characters, such as, per cent diosgenincontent in tubers, stem thickness and leaf breadth were fairlystable traits. Other characters, i.e. tuber length, tuber branchingand petiole length were not stable and were greatly influencedby the environment. The stability of fifteen genotypes variesfrom character to character and six genotypes were found tobe most stable for the majority of the characters. The significantgenotypic regression on the environment indicated that it shouldnot be difficult to breed D. deltoidea strains which shouldperform fairly well under diverse environmental conditions andto recognize the most desirable properties of a genotype tobe released as a variety for wide cultivation. Diosgenin, stable traits, heritable characters, environmental effect, adaptive genotypes     

RESPONSE TO NATURAL ENVIRONMENTAL HETEROGENEITY: MATERNAL EFFECTS AND SELECTION ON LIFE-HISTORY CHARACTERS AND PLASTICITIES IN MIMULUS GUTTATUS

Recent studies in plant populations have found that environmental heterogeneity and phenotypic selection vary at local spatial scales. In this study, I ask if there is evolutionary change in response to environmental heterogeneity and, if so, whether the response occurs for characters or character plasticities. I used vegetative clones of Mimulus guttatus to create replicate populations of 75 genotypes. These populations were planted into the natural habitat where they differed in mean growth, flowering phenology, and life span. This phenotypic variation was used to define selective environments. There was variation in fitness (flower production) among genotypes across all planting sites and in genotype response to the selective environment. Offspring from each site were grown in the greenhouse in two water treatments. Because each population initially had the same genetic composition, variation in the progeny between selective environments reveals either evolutionary change in response to environmental heterogeneity or environmental maternal effects. Plants from experimental sites that flowered earlier, had shorter life spans and were less productive, produced offspring that had more flowers, on average, and were less plastic in vegetative allocation than offspring of longer-lived plants from high-productivity areas. However, environmental maternal effects masked phenotypic differences in flower production. Therefore, although there was evidence of genetic differentiation in both life-history characters and their plasticities in response to small-scale environmental heterogeneity, environmental maternal effects may slow evolutionary change. Response to local-scale selective regimes suggests that environmental heterogeneity and local variation in phenotypic selection may act to maintain genetic variation.     

A POPULATION GENETIC THEORY OF CANALIZATION

Canalization is the suppression of phenotypic variation. Depending on the causes of phenotypic variation, one speaks either of genetic or environmental canalization. Genetic canalization describes insensitivity of a character to mutations, and the insensitivity to environmental factors is called environmental canalization. Genetic canalization is of interest because it influences the availability of heritable phenotypic variation to natural selection, and is thus potentially important in determining the pattern of phenotypic evolution. In this paper a number of population genetic models are considered of a quantitative character under stabilizing selection. The main purpose of this study is to define the population genetic conditions and constraints for the evolution of canalization. Environmental canalization is modeled as genotype specific environmental variance. It is shown that stabilizing selection favors genes that decrease environmental variance of quantitative characters. However, the theoretical limit of zero environmental variance has never been observed. Of the many ways to explain this fact, two are addressed by our model. It is shown that a “canalization limit” is reached if canalizing effects of mutations are correlated with direct effects on the same character. This canalization limit is predicted to be independent of the strength of stabilizing selection, which is inconsistent with recent experimental data (Sterns et al. 1995). The second model assumes that the canalizing genes have deleterious pleiotropic effects. If these deleterious effects are of the same magnitude as all the other mutations affecting fitness very strong stabilizing selection is required to allow the evolution of environmental canalization. Genetic canalization is modeled as an influence on the average effect of mutations at a locus of other genes. It is found that the selection for genetic canalization critically depends on the amount of genetic variation present in the population. The more genetic variation, the stronger the selection for canalizing effects. All factors that increase genetic variation favor the evolution of genetic canalization (large population size, high mutation rate, large number of genes). If genetic variation is maintained by mutation-selection balance, strong stabilizing selection can inhibit the evolution of genetic canalization. Strong stabilizing selection eliminates genetic variation to a level where selection for canalization does not work anymore. It is predicted that the most important characters (in terms of fitness) are not necessarily the most canalized ones, if they are under very strong stabilizing selection (k > 0.2V_e). The rate of decrease of mutational variance V_m is found to be less than 10% of the initial V_m. From this result it is concluded that characters with typical mutational variances of about 10^–3 V_e are in a metastable state where further evolution of genetic canalization is too slow to be of importance at a microevolutionary time scale. The implications for the explanation of macroevolutionary patterns are discussed.     

GENOTYPE-ENVIRONMENT INTERACTION AND THE EVOLUTION OF PHENOTYPIC PLASTICITY

Studies of spatial variation in the environment have primarily focused on how genetic variation can be maintained. Many one-locus genetic models have addressed this issue, but, for several reasons, these models are not directly applicable to quantitative (polygenic) traits. One reason is that for continuously varying characters, the evolution of the mean phenotype expressed in different environments (the norm of reaction) is also of interest. Our quantitative genetic models describe the evolution of phenotypic response to the environment, also known as phenotypic plasticity (Gause, 1947), and illustrate how the norm of reaction (Schmalhausen, 1949) can be shaped by selection. These models utilize the statistical relationship which exists between genotype-environment interaction and genetic correlation to describe evolution of the mean phenotype under soft and hard selection in coarse-grained environments. Just as genetic correlations among characters within a single environment can constrain the response to simultaneous selection, so can a genetic correlation between states of a character which are expressed in two environments. Unless the genetic correlation across environments is ± 1, polygenic variation is exhausted, or there is a cost to plasticity, panmictic populations under a bivariate fitness function will eventually attain the optimum mean phenotype for a given character in each environment. However, very high positive or negative correlations can substantially slow the rate of evolution and may produce temporary maladaptation in one environment before the optimum joint phenotype is finally attained. Evolutionary trajectories under hard and soft selection can differ: in hard selection, the environments with the highest initial mean fitness contribute most individuals to the mating pool. In both hard and soft selection, evolution toward the optimum in a rare environment is much slower than it is in a common one. A subdivided population model reveals that migration restriction can facilitate local adaptation. However, unless there is no migration or one of the special cases discussed for panmictic populations holds, no geographical variation in the norm of reaction will be maintained at equilibrium. Implications of these results for the interpretation of spatial patterns of phenotypic variation in natural populations are discussed.     

Spatial patterns in the distributions of polygenic characters

The spatial patterns in the mean and variance of a quantitative character that result from the interaction of spatially varying, optimizing selection and gene flow are considered. The model analyzed is an extension of those of Kimura (1965) and Lande (1976) for the distribution of a quantitative character maintained in a population by independent mutations. For weak selection, it is shown that there is only a small effect of gene flow on the variance of the character and that the mean value changes on a length scale that is large compared to the average dispersal distance. As in models of clines in allele frequencies, it is possible to define a “characteristic length” in terms of the average dispersal distance and strength of selection. The characteristic length is the smallest length scale environmental change to which the mean value of the character can significantly respond. It is also shown that, for weak selection, an asymmetry in dispersal can result in a significant shift in location of a cline. By considering an infinite linear cline in optimal values, it is shown that gene flow can increase the variance only when there is sufficient mixing in each generation of individuals from locations with different means. A model of selection in different niches is also considered. There is an increase in variance due to the effective weakening of the intensity of selection because of the differences in optimal values in different niches.The implications of the different models for maintenance of genetic polymorphism are discussed. Under some conditions gene flow can produce a significant increase in heterozygosity. It is also argued that spatial variation in selection on a polygenic character can be much more effective in increasing heterozygosity than temporal variation because of the potentially greater increase in phenotypic variance. The difference between some of the results for polygenic characters from those of similar models of one and two locus systems is accounted for by the fact that for normally distributed polygenic characters, changes in the variance are effectively decoupled from changes in the mean.     

How many processes are responsible for phenotypic evolution?

SUMMARY In addressing phenotypic evolution, this article reconsiders natural selection, random drift, developmental constraints, and internal selection in the new extended context of evolutionary developmental biology. The change of perspective from the "evolution of phenotypes" toward an "evolution of ontogenies" (evo-devo perspective) affects the reciprocal relationships among these different processes. Random drift and natural selection are sibling processes: two forms of post-productional sorting among alternative developmental trajectories, the former random, the latter nonrandom. Developmental constraint is a compound concept; it contains even some forms of natural ("external" and "internal") selection. A narrower definition ("reproductive constraints") is proposed. Internal selection is not a selection caused by an internal agent. It is a form of environment-independent selection depending on the level of the organism's internal developmental or functional coordination. Selection and constraints are the main deterministic processes in phenotypic evolution but they are not opposing forces. Indeed, they are continuously interacting processes of evolutionary change, but with different roles that should not be confused.     

Pleiotropic mutation, modularity and evolvability

The relationship between pleiotropy and the rate of evolution of a phenotypic character (evolvability) in a population is explored using computer simulations. I present results that suggest the rate of evolution of a phenotypic character may not decline when that character is pleiotropically associated to an increasing number of other characters, provided that the characters are under pure directional selection such that they are far from their optima relative to the average magnitude of a mutation. These conditions may be relevant during adaptive radiations. Adding pleiotropic associations to a set of characters in which one is under directional selection and the other is under stabilizing selection increases the rate of adaptation of the character under directional selection provided that the new characters that come to be pleiotropically associated are under directional selection. Thus, increasing the number of pleiotropic associations under these conditions increases the rate of adaptation of a character.     

Morphological variation over ontogeny and environments in resource polymorphic arctic charr (Salvelinus alpinus)

SUMMARY Natural selection requires genetically based phenotypic variation to facilitate its action and cause adaptive evolution. It has become increasingly recognized that morphological development can become canalized likely as a result of selection. However, it is largely unknown how selection may influence canalization over ontogeny and differing environments. Changes in environments or colonization of a novel one is expected to result in adaptive divergence from the ancestral population when selection favors a new phenotypic optimum. In turn, a novel environment may also expose variation previously hidden from natural selection. We tested for changes in phenotypic variation over ontogeny and environments among ecomorphs of Arctic charr (Salvelinus alpinus) from two Icelandic lakes. Populations represented varying degrees of ecological specialization, with one lake population possessing highly specialized ecomorphs exhibiting a large degree of phenotypic divergence, whereas the other displayed more subtle divergence with more ecological overlap. Here we show that ecomorphs hypothesized to be the most specialized in each lake possess significant reductions in shape variation over ontogeny regardless of environmental treatment suggesting canalized development. However, environments did change the amount of shape variation expressed in these ecomorphs, with novel environments slowing the rate at which variation was reduced over ontogeny. Thus, environmental conditions may play an important role in determining the type and amount of genetically based phenotypic variation exposed to natural selection.     

The fitness costs of developmental canalization and plasticity

Organisms are capable of an astonishing repertoire of phenotypic responses to the environment, and these often define important adaptive solutions to heterogeneous and unpredictable conditions. The terms ‘phenotypic plasticity’ and ‘canalization’ indicate whether environmental variation has a large or small effect on the phenotype. The evolution of canalization and plasticity is influenced by optimizing selection‐targeting traits within environments, but inherent fitness costs of plasticity may also be important. We present a meta‐analysis of 27 studies (of 16 species of plant and 7 animals) that have measured selection on the degree of plasticity independent of the characters expressed within environments. Costs of plasticity and canalization were equally frequent and usually mild; large costs were observed only in studies with low sample size. We tested the importance of several covariates, but only the degree of environmental stress was marginally positively related to the cost of plasticity. These findings suggest that costs of plasticity are often weak, and may influence phenotypic evolution only under stressful conditions.     

Disruptive selection on female reproductive characters in a hybrid zone of Littorina saxatilis

We studied natural selection in a hybrid zone of the intertidal marine snail Littorina saxatilis located in Galicia (NW Spain) by measuring the number and average size of the embryos carried by females. We related these characters with the females' position on the phenotypic and environmental gradients between the two pure morphs of the hybrid zone. In contrast with previous interpretations of studies made in this hybrid zone, we found a depression in both embryo number and size for phenotypically intermediate females. This disruptive natural selection could play an important role in the maintenance of the population's bimodal phenotypic distribution and in that of the assortative mating between the pure morphs. We found also that intermediate environments tended to be unfavorable for all phenotypes. Although the precise causes for the found depression in female reproductive characters remain to be determined, these results serve to emphasize the importance of studying whole fitness surfaces in hybrid zones, across the complete phenotypic and environmental ranges, instead of merely comparing the fitness averages of the two pure morphs and the intermediate individuals, taken as three discrete phenotypic classes.     

Climatic and temporal effects on the expression of secondary sexual characters: genetic and environmental components

Despite great interest in sexual selection, relatively little is known in detail about the genetic and environmental determinants of secondary sexual characters in natural populations. Such information is important for determining the way in which populations may respond to sexual selection. We report analyses of genetic and large-scale environmental components of phenotypic variation of two secondary sexual plumage characters (forehead and wing patch size) in the collared flycatcher Ficedula albicollis over a 22-year period. We found significant heritability for both characters but little genetic covariance between the two. We found a positive association between forehead patch size and a large-scale climatic index, the North Atlantic Oscillation (NAO) index, but not for wing patch. This pattern was observed in both cross-sectional and longitudinal data suggesting that the population response to NAO index can be explained as the result of phenotypic plasticity. Heritability of forehead patch size for old males, calculated under favorable conditions (NAO index > or = median), was greater than that under unfavorable conditions (NAO index < median). These changes occurred because there were opposing changes in additive genetic variance (VA) and residual variance (VR) under favorable and unfavorable conditions, with VA increasing and VR decreasing in good environments. However, no such effect was detected for young birds, or for wing patch size in either age class. In addition to these environmental effects on both phenotypic and genetic variances, we found evidence for a significant decrease of forehead patch size over time in older birds. This change appears to be caused by a change in the sign of viability selection on forehead patch size, which is associated with a decline in the breeding value of multiple breeders. Our data thus reveal complex patterns of environmental influence on the expression of secondary sexual characters, which may have important implications for understanding selection and evolution of these characters.     

Evolution of a plastic quantitative trait in an age-structured population in a fluctuating environment

We analyze weak fluctuating selection on a quantitative character in an age-structured population not subject to density regulation. We assume that early in the first year of life before selection, during a critical state of development, environments exert a plastic effect on the phenotype, which remains constant throughout the life of an individual. Age-specific selection on the character affects survival and fecundity, which have intermediate optima subject to temporal environmental fluctuations with directional selection in some age classes as special cases. Weighting individuals by their reproductive value, as suggested by Fisher, we show that the expected response per year in the weighted mean character has the same form as for models with no age structure. Environmental stochasticity generates stochastic fluctuations in the weighted mean character following a first-order autoregressive model with a temporally autocorrelated noise term and stationary variance depending on the amount of phenotypic plasticity. The parameters of the process are simple weighted averages of parameters used to describe age-specific survival and fecundity. The "age-specific selective weights" are related to the stable distribution of reproductive values among age classes. This allows partitioning of the change in the weighted mean character into age-specific components.     

Evolutionary Analyses of Morphological and Physiological Plasticity in Thermally Variable Environments

SYNOPSIS. Morphological and physiological plasticity is oftenthought to represent an adaptive response to variable environments.However, determining whether a given pattern of plasticity isin fact adaptive is analytically challenging, as is evaluatingthe degree of and limits to adaptive plasticity. Here we describea general methodological framework for studying the evolutionof plastic responses. This framework synthesizes recent analyticaladvances from both evolutionary ecology and functional biology,and it does so by integrating field experiments, functionaland physiological analyses, environmental data, and geneticstudies of plasticity. We argue that studies of plasticity inresponse to the thermal environment may be particularly valuablein understanding the role of environmental variation in theevolution of plasticity: not only can thermally-relevant traitsoften be mechanistically and physiologically linked to the thermalenvironment, but also the variability and predictability ofthe thermal environment itself can be quantified on ecologicallyrelevant time scales. We illustrate this approach by reviewinga case study of seasonal plasticity in the extent of wing melanizationin Western White Butterflies (Pontia occidentalis). This reviewdemonstrates that 1) wing melanin plasticity is heritable, 2)plasticity does increase fitness in nature, but the effect variesbetween seasons and between years, 3) selection on existingvariation in the magnitude of plasticity favors increased plasticityin one melanin trait that affects thermoregulation, but 4) themarked unpredictability of short-term (within-season) weatherpatterns substantially limits the capacity of plasticity tomatch optimal wing phenotypes to the weather conditions actuallyexperienced. We complement the above case study with a casualreview of selected aspects of thermal acclimation responses.The magnitude of thermal acclimation ("flexibility") is demonstrablymodest rather than fully compensatory. The magnitude of geneticvariation (crucial to evolutionary responses to selection) inthermal acclimation responses has been investigated in onlya few species to date. In conclusion, we suggest that an understandingof selection and evolution of thermal acclimation will be enhancedby experimental examinations of mechanistic links between traitsand environments, of the physiological bases and functionalconsequences of acclimation, of patterns of environmental variabilityand predictability, of the fitness consequences of acclimationin nature, and of potential genetic constraints.     

PHENOTYPIC PLASTICITY IN POLYGONUM PERSICARIA. I. DIVERSITY AND UNIFORMITY IN GENOTYPIC NORMS OF REACTION TO LIGHT

Several aspects of genotype-environment interaction may act to modulate natural selection in populations that encounter variable environments. In this study the norms of reaction (phenotypic responses) of 20 cloned genotypes from two natural populations of the annual plant Polygonum persicaria were determined over a broad range of controlled light environments (8%-100% full sun). These data reveal both the extent of functionally adaptive phenotypic plasticity expressed by individual genotypes, and the patterns of diversity among genotypes for characters relevant to fitness, in response to an environmental factor that is both highly variable within populations and critical to growth and reproduction.     

Differentiation and Stability in the Development of Nicotiana rustica

Stability, or homeostasis, is that property of the organismbuffering it against small random fluctuations of the environmentand accidents of development. A means of measuring, within theindividual, the stability of expression of one foliar and twofloral characters is given. Data are presented from a set of diallel crosses among fivevarieties of Nicotiana rustica, derived from different populationsand grown in two successive seasons. This allows stability tobe examined over a number of genotypes in the parent and F₁generations, in two differing environments. The leaf characters show some change from node to node, i.e.manifesting a gradual differentiation, as well as random fluctuationswhich are taken as evidence of instability. Like stability,this differentiation rate varies from genotype to genotype andshows genetic control. Some attempt is made to find to what extent the different phenomenaare related.     

Spatial variation in phenotypic selection on floral characteristics in an epiphytic orchid

Spatial variation in twelve floral characters was examined in an epiphytic orchidLepanthes rupestris to evaluate the strength and direction of phenotypic selection in seven riparian populations along two river basins in the Caribbean National Forest “El Yunque” for a range of 18–34 months. We evaluated selection on floral characters based on male (pollinaria removal) and female fitness (fruit set). Simple linear and quadratic regressions were used to evaluate the strength of directional, disruptive and stabilizing selections. Univariate and multivariate analyses were used to estimate the total strength of the selection acting on a character. Phenotypic selection was inconsistent among characters and populations. Few of the characters appeared to be under selection and none of them was found to be consistent throughout all populations. Inconsistency in selection coefficients among populations could suggest that selection is spatially variable. We only noted one character (column length) which had some consistency in differential selection coefficients among populations. Previous studies have shown that effective population sizes inL. rupestris are small and the observed “fitness differences” among populations could as easily be explained as stochastic events at play. We argue that the observed “fitness differences” in most characters and inconsistency among populations are likely from stochastic noise and not phenotypic selection. Consequently, we propose that random selection on character state support the hypothesis of genetic drift in small orchid populations.     

SELECTION FOR NATIVE CHARACTERS IN HYBRIDS BETWEEN TWO LOCALLY ADAPTED PLANT SUBSPECIES

Gene exchange between locally adapted plant populations can have significant evolutionary consequences, including changes in genetic diversity, introduction of adaptive or maladaptive traits, disruptive of coadaptive gene complexes, and the creation of new ecotypes or even species. The potential for introgression between divergent populations will depend on the strength of selection against nonnative characters. Morphologically variable F₂ hybrids of two Gilia capitata subspecies were used to evaluate the strength of phenotypic selection and the response to selection in the home habitats of each subspecies. At both sites, traits diagnostic of the subspecies were subject to significant phenotypic selection, probably mediated by direct selection on unmeasured correlated characters. Phenotypic selection favored native morphologies in all but a single case; leaf shape of one subspecies was favored in both habitats. The strength of selection varied between sites, with one site selecting more strongly against nonnative characters. Offspring of the F₂ hybrids showed a significant evolutionary response to selection when grown in a common environment. Evolution was in the direction of similarity with the subspecies native to the site where selection was imposed. This result reveals that native character states are adaptive and suggests that selection will maintain native morphologies even after a substantial influx of genes from an ecologically and morphologically distinct, and locally adapted subspecies.     

MEASURING NATURAL SELECTION ON PHENOTYPIC PLASTICITY

To understand natural selection we need to integrate its measure across environments. We present a method for measuring phenotypic selection that combines the potential for both environmental variation and phenotypic plasticity. The method uses path analysis and a measure of selection that is analogous to selection on breeding values. For individuals growing in alternative environments, paths are created that represent potential changes in the environment. The probabilities for these changes are then multiplied by the path coefficients to calculate selection coefficients. Selection on plasticity is measured as the difference in selection within each environment. We illustrate these methods using data on selection in an experimental population of Arabidopsis thaliana. Individuals from 36 families were grown in one of four environments, a factorial combination of shaded/open and early/late shading. For final height of the inflorescence, there was positive selection in both the open and shaded environments and negative selection on plasticity of height. For bolting time, there was also positive selection in both environments, but no selection on plasticity. We show how to use this information to examine how selection would change with changes in environmental frequencies and their transition probabilities. These methods can be expanded to encompass continuous traits and continuous environments as well as other complexities of natural selection.