The genetics of phenotypic plasticity I. Heritability

Methods for estimating the genetic component of phenotypic plasticity are presented. In the general case of clonal replicates or full-sibs raised in several environments, the heritability of plasticity can be measured as the ratio of the genotype-environment interaction variance to the total phenotypic variance. In the special case of only two environments plasticity also can be measured as the difference among environments in genotype or family means. In that case, the heritability of plasticity can be measured as either a ratio of variance components or as the slope of a parent-offspring regression. The general measure suffers because no least-square standard errors have been developed, although they can be calculated by maximum-likelihood or bootstrapping techniques. For the other two methods least-square standard errors can be calculated but require very large experiments for statistical significance to be achieved. The heritability measures are compared using data on plasticity of thorax size in response to temperature in Drosophila melanogaster. The heritability estimates are all in close agreement. Models of the evolution of phenotypic plasticity have treated it as a trait in its own right and as a cross-environment genetic correlation. Although the first approach is the one used here, neither one is preferred.     

The genetics of phenotypic plasticity. III. Genetic correlations and fluctuating asymmetries

We examined the relationship of three aspects of development, phenotypic plasticity, genetic correlations among traits, and developmental noise, for thorax length, wing length, and number of sternopleural bristles in Drosophila melanogaster. We used 14 lines which had previously been selected on either thorax length or plasticity of thorax length in response to temperature. A half-sib mating design was used and offspring were raised at 19° C or 25° C. We found that genetic correlations were stable across temperatures despite the large levels of plasticity of these traits. Plasticities were correlated among developmentally related traits, thorax and wing length, but not among unrelated traits, lengths and bristle counts. Amount of developmental noise, measured as fluctuating asymmetry and within-environmental variation, was positively correlated with amount of plasticity only for some traits, thorax length and bristle number, and only at one temperature, 25° C.     

Evolutionary genetics of Drosophila ananassae. I. Effect of selection on body size and inversion frequencies

Adaptive importance of inversion polymorphism has been discussed in Drosophila species at several levels but no study has been carried out demonstrating the individual and combined effects of polymorphic inversions on the fitness of flies through bi‐directional selection. Therefore, artificial bi‐directional selection for thorax length in Drosophila ananassae was carried out for 10 generations. Both, Tukey test for selection difference and regression coefficients of offspring on mid‐parent are highly significant. The realized heritability (h²) in males of both high and low selection lines is more or less similar but is more pronounced in low line females, which suggests the asymmetrical response. This asymmetry in selection is discussed in the light of evidence provided by the study of chromosome inversion frequencies in different selection lines at different generations of selection. Interestingly, chromosome inversion frequency changes towards homozygosity for different gene arrangements in different selection lines. Tests of correlations at G₆ and G₁₀ among different gene arrangements as well as with mean thorax length suggest that 2L‐ST gene arrangement is negatively correlated, while 3L‐ST gene arrangement is positively correlated with thorax length. Furthermore, the present study shows the significant effects of 3L‐ST and 2L + 3L (positive correlation) on thorax length, while 3R‐ST and 2L + 3R show significant effect (negative correlation) on thorax length, which was not evident in the previous study. Present results also suggest how polymorphic inversions and their combinations affect the body size differently in different selection lines. These results suggest that thorax length in D. ananassae is under polygenic control and inversion polymorphism plays crucial role in maintaining body size by modifying genotypic frequency under various selection pressures.     

Divergent selection and phenotypic plasticity during incipient speciation in Lake Victoria cichlid fish

Divergent selection acting on several different traits that cause multidimensional shifts are supposed to promote speciation, but the outcome of this process is highly dependent on the balance between the strength of selection vs. gene flow. Here, we studied a pair of sister species of Lake Victoria cichlids at a location where they hybridize and tested the hypothesis that divergent selection acting on several traits can maintain phenotypic differentiation despite gene flow. To explore the possible role of selection we tested for correlations between phenotypes and environment and compared phenotypic divergence (P_ST) with that based on neutral markers (F_ST). We found indications for disruptive selection acting on male breeding colour and divergent selection acting on several morphological traits. By performing common garden experiments we also separated the environmental and heritable components of divergence and found evidence for phenotypic plasticity in some morphological traits contributing to species differences.     

Selection experiments and the study of phenotypic plasticity1

Abstract Laboratory selection experiments are powerful tools for establishing evolutionary potentials. Such experiments provide two types of information, knowledge about genetic architecture and insight into evolutionary dynamics. They can be roughly classified into two types: (1) artificial selection in which the experimenter selects on a focal trait or trait index, and (2) quasi‐natural selection in which the experimenter establishes a set of environmental conditions and then allows the population to evolve. Both approaches have been used in the study of phenotypic plasticity. Artificial selection experiments have taken various forms including: selection directly on a reaction norm, selection on a trait in multiple environments, and selection on a trait in a single environment. In the latter experiments, evolution of phenotypic plasticity is investigated as a correlated response. Quasi‐natural selection experiments have examined the effects of both spatial and temporal variation. I describe how to carry out such experiments, summarize past efforts, and suggest further avenues of research.     

Evolution of adaptive phenotypic traits without positive Darwinian selection

Recent evidence suggests the frequent occurrence of a simple non-Darwinian (but non-Lamarckian) model for the evolution of adaptive phenotypic traits, here entitled the plasticity-relaxation-mutation (PRM) mechanism. This mechanism involves ancestral phenotypic plasticity followed by specialization in one alternative environment and thus the permanent expression of one alternative phenotype. Once this specialization occurs, purifying selection on the molecular basis of other phenotypes is relaxed. Finally, mutations that permanently eliminate the pathways leading to alternative phenotypes can be fixed by genetic drift. Although the generality of the PRM mechanism is at present unknown, I discuss evidence for its widespread occurrence, including the prevalence of exaptations in evolution, evidence that phenotypic plasticity has preceded adaptation in a number of taxa and evidence that adaptive traits have resulted from loss of alternative developmental pathways. The PRM mechanism can easily explain cases of explosive adaptive radiation, as well as recently reported cases of apparent adaptive evolution over ecological time.     

Phenotypic plasticity and selection in Drosophila life-history evolution. I. Nutrition and the cost of reproduction

Earlier experiments have shown that the evolution of postponed senescent populations can be achieved by selection on either demographic or stress resistance characters. Both types of selection have produced results in which survival characters (stress resistance and longevity) have apparently traded-off against early-life fecundity. Here we present the results of a series of experiments in which an environmental variable — the level of live yeast inoculate applied to the substrate — produces a qualitatively similar phenotypic response: longevity and starvation resistance are enhanced by lower yeast levels, at the expense of fecundity. For the starvation resistance versus fecundity experiments we show a negative and linear relationship between the norms of reaction for each character across a gradient of yeast levels. This phenotypic trade-off is stable across the 20 populations and 4 selection treatments reported on here, and its general agreement with earlier selection results suggests that the evolutionary response and the phenotypically plastic response may share a common physiological basis. However, an important discrepancy in the lifetime fecundity data between the selection response and the dietary manipulations preclude strict analogy. The results broadly conform to a simple “Y-model” of allocation, in which a limited resource is divided between survival and reproduction; here the characters are starvation resistance and longevity versus fecundity.     

Testing the adaptive plasticity of Iris pumila leaf traits to natural light conditions using phenotypic selection analysis

A multivariate selection analysis has been used to test the adaptiveness of several Iris pumila leaf traits that display plasticity to natural light conditions. Siblings of a synthetic population comprising 31 families of two populations from contrasting light habitats were grown at an open dune site and in the understory of a Pinus nigra stand in order to score variation in phenotypic expression of six leaf traits: number of senescent leaves, number of live leaves, leaf length, leaf width, leaf angle, and specific leaf area. The ambient light conditions affected the values of all traits studied except for specific leaf area. In accordance to ecophysiological expectations for an adaptive response to light, both leaf length and width were significantly greater while the angle between sequential leaves was significantly smaller in the woodland understory than at the exposed dune site. The relationship between leaf traits and vegetative fitness (total leaf area) differed across light habitats as predicted by functional hypotheses. The standardized linear selection gradient (β′) for leaf length and width were positive in sign in both environments, but their magnitude for leaf length was higher in the shade than under full sunlight. Since plasticity of leaf length in the woodland shade has been recognized as adaptive, fitness cost of producing plastic change in leaf length was assessed. In both of the available methods used, the two-step and the multivariate regression procedures, a rather high negative association between the fitness value and the plasticity of leaf length was obtained, indicating a cost of plasticity. The selection gradient for leaf angle was weak and significant only in the woodland understory. Genetic correlations between trait expressions in contrasting light environments were negative in sign and low in magnitude, implying a significant genetic variation for plasticity in these leaf traits. Furthermore, leaf length and leaf width were found to be genetically positively coupled, which indicates that there is a potential for these two traits to evolve toward their optimal phenotypic values even faster than would be expected if they were genetically independent.     

Correlated response in plasticity to selection for early flowering in Arabidopsis thaliana

Phenotypic plasticity is an important strategy for coping with changing environments. However, environmental change usually results in strong directional selection, and little is known empirically about how this affects plasticity. If genes affecting a trait value also affect its plasticity, selection on the trait should influence plasticity. Synthetic outbred populations of Arabidopsis thaliana were selected for earlier flowering under simulated spring- and winter-annual conditions to investigate the correlated response of flowering time plasticity and its effect on family-by-environment variance (Vg×e) within each selected line. We found that selection affected plasticity in an environmentally dependent manner: under simulated spring-annual conditions, selection increased the magnitude of plastic response but decreased Vg×e; selection under simulated winter-annual conditions reduced the magnitude of plastic response but did not alter Vg×e significantly. As selection may constrain future response to environmental change, the environment for crop breeding and ex situ conservation programmes should be carefully chosen. Models of species persistence under environmental change should also consider the interaction between selection and plasticity.     

Promising directions in plant phenotypic plasticity

A research agenda for the next phase of plasticity studies calls for contributions from a diverse group of biologists, working both independently and collaboratively, to pursue four promising directions: examining dynamic, anatomical/architectural, and cross-generational plasticity along with simpler growth traits; carefully assessing the adaptive significance of those plasticity patterns; investigating the intricate transduction pathways that lead from environmental signal to phenotypic response; and considering the rich environmental context of natural systems. Progress in these areas will allow us to address broad and timely questions regarding the ecological and evolutionary significance of plasticity and the nature of phenotypic determination.     

The evolution of phenotypic plasticity in spatially structured environments: implications of intraspecific competition, plasticity costs and environmental characteristics

We model the evolution of reaction norms focusing on three aspects: frequency-dependent selection arising from resource competition, maintenance and production costs of phenotypic plasticity, and three characteristics of environmental heterogeneity (frequency of environments, their intrinsic carrying capacity and the sensitivity to phenotypic maladaptation in these environments). We show that (i) reaction norms evolve so as to trade adaptation for acquiring resources against cost avoidance; (ii) maintenance costs cause reaction norms to better adapt to frequent rather than to infrequent environments, whereas production costs do not; and (iii) evolved reaction norms confer better adaptation to environments with low rather than with high intrinsic carrying capacity. The two previous findings contradict earlier theoretical results and originate from two previously unexplored features that are included in our model. First, production costs of phenotypic plasticity are only incurred when a given phenotype is actually produced. Therefore, they are proportional to the frequency of environments, and these frequencies thus affect the selection pressure to avoid costs just as much as the selection pressure to improve adaptation. This prevents the frequency of environments from affecting the evolving reaction norm. Secondly, our model describes the evolution of plasticity for a phenotype determining an individual's capability to acquire resources, and thus its realized carrying capacity. When individuals are distributed randomly across environments, they cannot avoid experiencing environments with intrinsically low carrying capacity. As selection pressures arising from the need to improve adaptation are stronger under such extreme conditions than under mild ones, better adaptation to environments with low rather than with high intrinsic carrying capacity results.     

A modular concept of phenotypic plasticity in plants

Based on empirical evidence from the literature we propose that, in nature, phenotypic plasticity in plants is usually expressed at a subindividual level. While reaction norms (i.e. the type and the degree of plant responses to environmental variation) are a property of genotypes, they are expressed at the level of modular subunits in most plants. We thus contend that phenotypic plasticity is not a whole-plant response, but a property of individual meristems, leaves, branches and roots, triggered by local environmental conditions. Communication and behavioural integration of interconnected modules can change the local responses in different ways: it may enhance or diminish local plastic effects, thereby increasing or decreasing the differences between integrated modules exposed to different conditions. Modular integration can also induce qualitatively different responses, which are not expressed if all modules experience the same conditions. We propose that the response of a plant to its environment is the sum of all modular responses to their local conditions plus all interaction effects that are due to integration. The local response rules to environmental variation, and the modular interaction rules may be seen as evolving traits targeted by natural selection. Following this notion, whole-plant reaction norms are an integrative by-product of modular plasticity, which has far-reaching methodological, ecological and evolutionary implications.     

Effects of spatial autocorrelation,natal philopatry and phenotypic plasticity on the heritability of laying date

We investigated the effect of spatial autocorrelation on heritability (h²) estimates of laying date and clutch size in a population of great tits Parus major. We found that h² of laying date, but not clutch size, declined significantly with increasing distance between the nestbox of mothers and daughters. This decline was caused by a decreasing effect of spatial autocorrelation in laying date, rather than by the existence of genotype–environment interactions (GEI). After correcting for the effect of spatial autocorrelation, h² of laying date was low (0.16 ± 0.07), but significant, and surprisingly consistent with increasing distance between parental and offspring environments. The h² of clutch size was not much affected by spatial autocorrelation. Most previously published estimates of the heritability of laying date include various degrees of common environment effects, which can bias estimates both upwards and downwards. We suggest that using techniques that take spatial autocorrelation into account might be a fruitful approach to estimate h² of traits that show a high degree of plasticity.     

Crest evolution in newts: implications for reconstruction methods, sexual selection, phenotypic plasticity and the origin of novelties

The dorsal crest of newts (Salamandridae) is a novel, phenotypically plastic, sexually selected trait that may evolve in association with complex courtship behaviours. We estimated a near-comprehensive, time-calibrated phylogeny for salamandrids and analysed the evolution of their crests and display behaviour. Different models give conflicting reconstructions for crest evolution, showing that likelihood can estimate incorrect ancestral states with strong statistical support. The best-fitting model suggests that crests evolved once and were lost repeatedly, supporting the hypothesis that sexually selected traits may be frequently lost. We demonstrate the correlated evolution of crests and courtship behaviour and show that species with larger numbers of crest-related traits have larger repertoires of behaviours. We also show that phenotypically plastic morphological traits can be maintained over long macroevolutionary timescales (～25-48 Myr). Finally, we use salamandrids to address how novel structures may arise, and support a model involving the expansion and subdivision of pre-existing structures.     

Environmental stress and the costs of whole-organism phenotypic plasticity in tadpoles

Costs of phenotypic plasticity are important for the evolution of plasticity because they prevent organisms from shaping themselves at will to match heterogeneous environments. These costs occur when plastic genotypes have relatively low fitness regardless of the trait value expressed. We report two experiments in which we measured selection on predator-induced plasticity in the behaviour and external morphology of frog tadpoles (Rana temporaria). We assessed costs under stressful and benign conditions, measured fitness as larval growth rate or competitive ability and focused analysis on aggregate measures of whole-organism plasticity. There was little convincing evidence for a cost of phenotypic plasticity in our experiments, and costs of canalization were nearly as frequent as costs of plasticity. Neither the magnitude of the cost nor the variation around the estimate (detectability) was sensitive to environmental stress.     

EVOLUTION AND DEVELOPMENT OF BODY SIZE AND CELL SIZE IN DROSOPHILA MELANOGASTER IN RESPONSE TO TEMPERATURE

We examined the evolutionary and developmental responses of body size to temperature in Drosophila melanogaster, using replicated lines of flies that had been allowed to evolve for 5 yr at 25°C or at 16.5°C. Development and evolution at the lower temperature both resulted in higher thorax length and wing area. The evolutionary effect of temperature on wing area was entirely a consequence of an increase in cell area. The developmental response was mainly attributable to an increase in cell area, with a small effect on cell number in males. Given its similarity to the evolutionary response, the increase in body size and cell size resulting from development at low temperature may be a case of adaptive phenotypic plasticity. The pattern of plasticity did not evolve in response to temperature for any of the traits. The selective advantage of the evolutionary and developmental responses to temperature is obscure and remains a major challenge for future work.     

How stress selects for reversible phenotypic plasticity

Stress occurring in periods shorter than life span strongly selects for reversible phenotypic plasticity, for maximum reliability of stress indicating cues and for minimal response delays. The selective advantage of genotypes that are able to produce adaptive reversible plastic phenotypes is calculated by using the concept of environmental tolerance. Analytic expressions are given for optimal values of mode and breadth of tolerance functions for stress induced and non-induced phenotypes depending on (1) length of stress periods, (2) response delay for switching into the induced phenotype, (3) response delay for rebuilding the non-induced phenotype, (4) intensity of stress, i.e. mean value of the stress inducing environment, (5) coefficient of variation of the stress environment and (6) completeness of information available to the stressed organism. Adaptively reversible phenotypic plastic traits will most probably affect fitness in a way that can be described by simultaneous reversible plasticity in mode and breadth of tolerance functions.     

Response of fluctuating and directional asymmetry to selection on wing shape in Drosophila melanogaster

We tested whether directional selection on an index-based wing character in Drosophila melanogaster affected developmental stability and patterns of directional asymmetry. We selected for both an increase (up selection) and a decrease (down selection) of the index value on the left wing and compared patterns of fluctuating and directional asymmetry in the selection index and other wing traits across selection lines. Changes in fluctuating asymmetry across selection lines were predominantly small, but we observed a tendency for fluctuating asymmetry to decrease in the up-selected lines in both replicates. Because changes in fluctuating asymmetry depended on the direction of selection, and were not related to changes in trait size, these results fail to support existing hypotheses linking directional selection and developmental stability. Selection also produced a pattern of directional asymmetry that was similar in all selected lines whatever the direction of selection. This result may be interpreted as a release of genetic variance in directional asymmetry under selection.