Phenotypic evolution in stochastic environments: The contribution of frequency- and density-dependent selection

Understanding how environmental variation affects phenotypic evolution requires models based on ecologically realistic assumptions that include variation in population size and specific mechanisms by which environmental fluctuations affect selection. Here we generalize quantitative genetic theory for environmentally induced stochastic selection to include general forms of frequency- and density-dependent selection. We show how the relevant fitness measure under stochastic selection relates to Fisher's fundamental theorem of natural selection, and present a general class of models in which density regulation acts through total use of resources rather than just population size. In this model, there is a constant adaptive topography for expected evolution, and the function maximized in the long run is the expected factor restricting population growth. This allows us to generalize several previous results and to explain why apparently “-selected” species with slow life histories often have low carrying capacities. Our joint analysis of density- and frequency-dependent selection reveals more clearly the relationship between population dynamics and phenotypic evolution, enabling a broader range of eco-evolutionary analyses of some of the most interesting problems in evolution in the face of environmental variation.     

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.     

Evolution in stressful environments II: adaptive value and costs of plasticity in response to low light in Sinapis arvensis

Plants possess a remarkable capacity to alter their phenotype in response to the highly heterogeneous light conditions they commonly encounter in natural environments. In the present study with the weedy annual plant Sinapis arvensis, we (a) tested for the adaptive value of phenotypic plasticity in morphological and life history traits in response to low light and (b) explored possible fitness costs of plasticity. Replicates of 31 half-sib families were grown individually in the greenhouse under full light and under low light (40% of ambient) imposed by neutral shade cloth. Low light resulted in a large increase in hypocotyl length and specific leaf area (SLA), a reduction in juvenile biomass and a delayed onset of flowering. Phenotypic selection analysis within each light environment revealed that selection favoured large SLA under low light, but not under high light, suggesting that the observed increase in SLA was adaptive. In contrast, plasticity in the other traits measured was maladaptive (i.e. in the opposite direction to that favoured by selection in the low light environment). We detected significant additive genetic variance in plasticity in most phenotypic traits and in fitness (number of seeds). Using genotypic selection gradient analysis, we found that families with high plasticity in SLA had a lower fitness than families with low plasticity, when the effect of SLA on fitness was statistically kept constant. This indicates that plasticity in SLA incurred a direct fitness cost. However, a cost of plasticity was only expressed under low light, but not under high light. Thus, models on the evolution of phenotypic plasticity will need to incorporate plasticity costs that vary in magnitude depending on environmental conditions.     

Natural selection, evolvability and bias due to environmental covariance in the field in an annual plant

Estimates of the form and magnitude of natural selection based on phenotypic relationships between traits and fitness measures can be biased when environmental factors influence both relative fitness and phenotypic trait values. I quantified genetic variances and covariances, and estimated linear and quadratic selection coefficients, for seven traits of an annual plant grown in the field. For replicates of 50 paternal half-sib families, coefficients of selection were calculated both for individual phenotypic values of the traits and for half-sib family mean values. The potential for evolutionary response was supported by significant heritability and phenotypic directional selection for several traits but contradicted by the absence of significant genetic variation for fitness estimates and evidence of bias in phenotypic selection coefficients due to environmental covariance for at least two of the traits analysed. Only studies of a much wider range of organisms and traits will reveal the frequency and extent of such bias.     

Evolution of the environmental component of the phenotypic variance: stabilizing selection in changing environments and the cost of homogeneity

Quantitative traits show abundant genetic, environmental, and phenotypic variance, yet if they are subject to stabilizing selection for an optimal phenotype, both the genetic and environmental components are expected to decline. The mechanisms that determine the level and maintenance of phenotypic variance are not yet fully understood. While there has been extensive study of mechanisms maintaining genetic variability, it has generally been assumed that environmental variance is not dependent on the genotype and therefore not subject to change. However, accumulating data suggest that the environmental variance is under some degree of genetic control. In this study, it is assumed accordingly that both the genotypic value (i.e., mean phenotypic value) and the variance of phenotypic value given genotypic value depend on the genotype. Two models are investigated as potentially able to explain the protected maintenance of environmental variance of quantitative traits under stabilizing selection. One is varying environment among generations, such that both the optimal phenotype and the strength of the stabilizing selection vary between generations. The other is the cost of homogeneity, which is based on an assumption of an engineering cost of minimizing variability in development. It is shown that a small homogeneity cost is enough to maintain the observed levels of environmental variance, whereas a large amount of temporal variation in the optimal phenotype and the strength of selection would be necessary.     

Phenotypic plasticity for life history traits in Drosophila melanogaster. I. Effect on phenotypic and environmental correlations

All 36 possible crosses among 6 homozygous lines of Drosophila melanogaster were tested for their phenotypic response in developmental time and dry weight at eclosion to variation in temperature and yeast concentration. This method was chosen because it allows one to produce the same heterozygous offspring repeatedly for testing under more conditions than could be handled at once. We estimated the effects of yeast concentration and temperature and their interaction on both the phenotypic and the environmental components of variation and covariation of the two traits. Development was slower at low temperatures and yeast concentrations, and dry weight and viability were lower at higher temperatures and lower yeast levels. Interactions of the two factors with the crosses and with each other indicated that there were genetic differences in plasticity and that the sensitivity of a trait to one factor depended on the level of the other. The covariation of the two traits was generally weak within an environment. Across environments, its sign depended on the factor that changed between the environments: positive for temperature, negative for yeast concentration. These findings can be explained in terms of an established growth model for Drosophila larvae. We conclude that for plastic traits with moderate or low heritability, the relationship between the phenotypic and genetic covariance matrices may be a complex function of the environmental factors that affect the traits. Some implications for the prediction of the evolution in fluctuating environments are outlined.     

Genotype-by-environment interactions leads to variable selection on life-history strategy in Common Evening Primrose (Oenothera biennis)

Monocarpic plant species, where reproduction is fatal, frequently exhibit variation in the length of their prereproductive period prior to flowering. If this life-history variation in flowering strategy has a genetic basis, genotype-by-environment interactions (G x E) may maintain phenotypic diversity in flowering strategy. The native monocarpic plant Common Evening Primrose (Oenothera biennis L., Onagraceae) exhibits phenotypic variation for annual vs. biennial flowering strategies. I tested whether there was a genetic basis to variation in flowering strategy in O. biennis, and whether environmental variation causes G x E that imposes variable selection on flowering strategy. In a field experiment, I randomized more than 900 plants from 14 clonal families (genotypes) into five distinct habitats that represented a natural productivity gradient. G x E strongly affected the lifetime fruit production of O. biennis, with the rank-order in relative fitness of genotypes changing substantially between habitats. I detected genetic variation in annual vs. biennial strategies in most habitats, as well as a G x E effect on flowering strategy. This variation in flowering strategy was correlated with genetic variation in relative fitness, and phenotypic and genotypic selection analyses revealed that environmental variation resulted in variable directional selection on annual vs. biennial strategies. Specifically, a biennial strategy was favoured in moderately productive environments, whereas an annual strategy was favoured in low-productivity environments. These results highlight the importance of variable selection for the maintenance of genetic variation in the life-history strategy of a monocarpic plant.     

Cloning and expression pattern of heat shock protein genes from the endoparasitoid wasp, Pteromalus puparum in response to environmental stresses

Six heat shock protein (HSP) genes from five HSP families in the parasitoid, Pteromalus puparum, were evaluated for their response to temperature (-15 ~ 3°C , and 30 ~ 42°C for 1 h), heavy metals (0.5 ~ 5 mM Cd(2+) and Cu(2+) for 24 h and 60 h), and starvation (24 h). Compared with other insect HSPs, all conserved motifs are found in P. puparum HSPs, and they are very similar to those of the recently sequenced ectoparasitoid Nasonia vitripennis. The temporal gene expression patterns indicated that these six HSP genes were all heat-inducible, of which hsp40 was the most inducible. The temperatures for maximal HSP induction at high and low temperature zone were 36 or 39°C and -3°C, respectively. In the hot zone, all HSP genes have the same initial temperature (33°C) for up-regulation. Low concentrations of Cd(2+) for a short-term promoted the expression of all HSP genes, but not high concentrations or long-term treatments. Cu(2+) stress for 24 h increased expression of nearly all HSP. Four HSP genes changed after starvation. We infer that all six HSP genes are sensitive to heat. This may help understand the absence of P. puparum during the summer and winter. The expression profiles of six HSP genes in P. puparum under heavy metal stress indicates that HSP is a short-term response to cellular distress or injury induced by Cd(2+) and Cu(2+).     

Correlated responses to artificial body size selection in growth, development, phenotypic plasticity and juvenile viability in yellow dung flies

Most life history traits are positively influenced by body size, whereas disadvantages of large body size are poorly documented. To investigate presumed intrinsic costs of large size in the yellow dung fly (Scathophaga stercoraria; Diptera: Scathophagidae), we established two replicates each of three body size laboratory selection lines (small, control and large; selection on males only), and subjected flies of the resulting extended body size range to various abiotic stresses. Response to selection was symmetrical in the small and large lines (realized h(2) = 0.16-0.18). After 24 generations of selection body size had changed by roughly 10%. Female size showed a correlated response to selection on male size, whereas sexual size dimorphism did not change. Development time also showed a correlated response as, similar to food limited flies, small line flies emerged earlier at smaller body size. At the lowest larval food limit possible, flies of all lines emerged at the same small body size after roughly the same development time; so overall phenotypic plasticity in body size and development time strongly increased following selection. Juvenile mortality increased markedly when food was extremely limited, large line flies showing highest mortality. Winter frost disproportionately killed large (line) flies because of their longer development times. Mortality at high temperatures was high but size-selective effects were inconsistent. In all environments the larger males suffered more. Initial growth rate was higher for males and at unlimited food. Small line individuals of both sexes grew slowest at unlimited larval food but fastest at limited larval food, suggesting a physiological cost of fast growth. Overall, extension of the natural body size range by artificial selection revealed some otherwise cryptic intrinsic juvenile viability costs of large size, mediated by longer development or faster growth, but only in stressful environments.     

Natural variation,differentiation, and genetic trade‐offs of ecophysiological traits in response to water limitation in Brachypodium distachyon and its descendent allotetraploid B. hybridum (Poaceae)

Differences in tolerance to water stress may underlie ecological divergence of closely related ploidy lineages. However, the mechanistic basis of physiological variation governing ecogeographical cytotype segregation is not well understood. Here, using Brachypodium distachyon and its derived allotetraploid B. hybridum as model, we test the hypothesis that, for heteroploid annuals, ecological divergence of polyploids in drier environments is based on trait differentiation enabling drought escape. We demonstrate that under water limitation allotetraploids maintain higher photosynthesis and stomatal conductance and show earlier flowering than diploids, concordant with a drought‐escape strategy to cope with water stress. Increased heterozygosity and greater genetic variability and plasticity of polyploids could confer a superior adaptive capability. Consistent with these predictions, we document (1) greater standing within‐population genetic variation in water‐use efficiency (WUE) and flowering time in allotetraploids, and (2) the existence of (nonlinear) environmental clines in physiology across allotetraploid populations. Increased gas exchange and diminished WUE occurred at the driest end of the gradient, consistent with a drought‐escape strategy. Finally, we found that allotetraploids showed weaker genetic correlations than diploids congruous with the expectation of relaxed pleiotropic constraints in polyploids. Our results suggest evolutionary divergence of ecophysiological traits in each ploidy lineage.