On the evolution of mutation in changing environments: recombination and phenotypic switching

Phenotypic switching has been observed in laboratory studies of yeast and bacteria, in which the rate of such switching appears to adjust to match the frequency of environmental changes. Among possible mechanisms of switching are epigenetic influences on gene expression and variation in levels of methylation; thus environmental and/or genetic factors may contribute to the rate of switching. Most previous analyses of the evolution of phenotypic switching have compared exponential growth rates of noninteracting populations, and recombination has been ignored. Our genetic model of the evolution of switching rates is framed in terms of a mutation-modifying gene, environments that cause periodic changes in fitness, and recombination between the mutation modifier and the gene under selection. Exact results are obtained for all recombination rates and symmetric fitnesses that strongly generalize earlier results obtained under complete linkage and strong constraints on the relation between fitness and period of switching. Our analytical and numerical results suggest a general principle that recombination reduces the stable rate of switching in symmetric and asymmetric fitness regimes and when the period of switching is random. As the recombination rate increases, it becomes less likely that there is a stable nonzero rate of switching.     

Evolution in heterogeneous environments and the potential of maintenance of genetic variation in traits of adaptive significance

The maintenance of genetic variation in traits of adaptive significance has been a major dilemma of evolutionary biology. Considering the pattern of increased genetic variation associated with environmental clines and heterogeneous environments, selection in heterogeneous environments has been proposed to facilitate the maintenance of genetic variation. Some models examining whether genetic variation can be maintained, in heterogeneous environments are reviewed. Genetic mechanisms that constrain evolution in quantitative genetic traits indicate that genetic variation can be maintained but when is not clear. Furthermore, no comprehensive models have been developed, likely due to the genetic and environmental complexity of this issue. Therefore, I have suggested two empirical approaches to provide insight for future theoretical and empirical research. Traditional path analysis has been a very powerful approach for understanding phenotypic selection. However, it requires substantial information on the biology of the study system to construct a causal model and alternatives. Exploratory path analysis is a data driven approach that uses the statistical relationships in the data to construct a set of models. For example, it can be used for understanding phenotypic selection in different environments, where there is no prior information to develop path models in the different environments. Data from Brassica rapa grown in different nutrients indicated that selection changed in the different environments. Experimental evolutionary studies will provide direct tests as to when genetic variation is maintained.     

Sex ratio variance and the maintenance of environmental sex determination

Although variation in population sex ratios is predicted to increase the extinction rate of clades with environmental sex determination (ESD), ESD is still seen in a wide array of natural systems. It is unclear how this common sex-determining system has persisted despite this inherent disadvantage associated with ESD. We use simulation modelling to examine the effect of the sex ratio variance caused by ESD on population colonization and establishment. We find that an accelerating function of establishment success on initial population sex ratio favours a system that produces variance in sex ratios over one that consistently produces even sex ratios. This sex ratio variance causes ESD to be favoured over genetic sex determination, even when the mean global sex ratio under both sex-determining systems is the same. Data from ESD populations suggest that the increase in population establishment can more than offset the increased risk of extinction associated with temporal fluctuations in the sex ratio. These findings demonstrate that selection in natural systems can favour increased variance in a trait, irrespective of the mean trait value. Our results indicate that sex ratio variation may provide an advantage to species with ESD, and may help explain the widespread existence of this sex-determining system.     

Regulation of diversity: maintenance of species richness in changing environments

In order to assess how diversity changes over time at sites undergoing environmental change, we examined three data sets on long-term trends in taxonomic richness and composition: (1) 22 years of rodent censuses from a site in the Chihuahuan Desert of Arizona; (2) 50 years of bird surveys from a three-county region of northern Michigan; and (3) approximately 10,000 years of pollen records from two sites in Europe. In all three cases, richness has remained remarkably constant despite large changes in composition. The results suggest that while species composition may be highly variable and change substantially in response to environmental change, species diversity is an emergent property of ecosystems that is often maintained within narrow limits. Such regulation of diversity requires maintenance of relatively constant levels of productivity and resource availability and an open system with opportunity for compensatory colonizations and extinctions. In addition to studying the effects of diversity on biogeochemical processes, it will often be useful to think of species richness as an emergent consequence of ecosystem processes.     

Dependence of phenotypic variance in body size on environmental quality

The recent "overhead threshold" model for optimal age and body size at maturity (Day and Rowe 2002 ) predicts that phenotypic variability in adult body size will be low under inferior environmental quality and will increase with improving conditions. The model is, however, based on a potentially restrictive assumption of a monotone increase of fecundity with increasing body size. On the basis of a numerical model, we show that introducing the concept of maximum adult body size changes the predictions of the model. The dependence of variability in adult body size on environmental quality becomes a concave function with a maximum at intermediate values. Depending on the range of environmental conditions considered, one may therefore expect to observe both increasing and decreasing functions. We test the predictions of our model on a literature-based database of 131 insect species covering all major orders. We demonstrate that, in most species, relative phenotypic variation in body size decreases when environment-specific average of adult body size increases. In the majority of cases at least, such a relationship can be interpreted as a decreased relative variation in better growing conditions. With some potentially meaningful exceptions (e.g., females of capital-breeding insects), the general pattern was largely invariable across different taxa, ecological subdivisions, and sexes.     

Sources of phenotypic variance in egg and larval traits in a marine invertebrate

Contrary to many separate sex systems, the evolutionary ecology of polyandry in simultaneous hermaphrodites, and in particular in those with internal fertilization, has received little attention. Recent studies on the promiscuous gastropod Chelidonura sandrana showed that offspring size, an important determinant of offspring performance in many marine invertebrates, varies with the number of different mating partners. However, the source of this differential allocation by mothers remained unclear. Using a quantitative genetic model, we here tested for parental effects on offspring size and the importance of ‘good gene’ effects on early life history traits. Our analysis revealed no significant sire but strong dam effects for all investigated traits. Moreover, embryo viability tended to increase with egg capsule volume, thus linking offspring size with offspring performance. Our findings suggest that in C. sandrana (1) differential allocation is a maternal effect in response to the number of different partners, and that (2) additive genetic variance is of negligible importance in early life history traits.     

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.     

Evolution of genetic variability and the advantage of sex and recombination in changing environments.

The role of recombination and sexual reproduction in enhancing adaptation and population persistence in temporally varying environments is investigated on the basis of a quantitative-genetic multilocus model. Populations are finite, subject to density-dependent regulation with a finite growth rate, diploid, and either asexual or randomly mating and sexual with or without recombination. A quantitative trait is determined by a finite number of loci at which mutation generates genetic variability. The trait is under stabilizing selection with an optimum that either changes at a constant rate in one direction, exhibits periodic cycling, or fluctuates randomly. It is shown by Monte Carlo simulations that if the directional-selection component prevails, then freely recombining populations gain a substantial evolutionary advantage over nonrecombining and asexual populations that goes far beyond that recognized in previous studies. The reason is that in such populations, the genetic variance can increase substantially and thus enhance the rate of adaptation. In nonrecombining and asexual populations, no or much less increase of variance occurs. It is explored by simulation and mathematical analysis when, why, and by how much genetic variance increases in response to environmental change. In particular, it is elucidated how this change in genetic variance depends on the reproductive system, the population size, and the selective regime, and what the consequences for population persistence are.     

Linking traits to energetics and population dynamics to predict lizard ranges in changing environments

I present a dynamic bioenergetic model that couples individual energetics and population dynamics to predict current lizard ranges and those following climate warming. The model predictions are uniquely based on first principles of morphology, life history, and thermal physiology. I apply the model to five populations of a widespread North American lizard, Sceloporus undulatus, to examine how geographic variation in traits and life histories influences ranges. This geographic variation reflects the potential for species to adapt to environmental change. I then consider the range dynamics of the closely related Sceloporus graciosus. Comparing predicted ranges and actual current ranges reveals how dispersal limitations, species interactions, and habitat requirements influence the occupied portions of thermally suitable ranges. The dynamic model predicts individualistic responses to a uniform 3 degrees C warming but a northward shift in the northern range boundary for all populations and species. In contrast to standard correlative climate envelope models, the extent of the predicted northward shift depends on organism traits and life histories. The results highlight the limitations of correlative models and the need for more dynamic models of species' ranges.     

Bayesian mapping of quantitative trait loci under the identity-by-descent-based variance component model

Variance component analysis of quantitative trait loci (QTL) is an important strategy of genetic mapping for complex traits in humans. The method is robust because it can handle an arbitrary number of alleles with arbitrary modes of gene actions. The variance component method is usually implemented using the proportion of alleles with identity-by-descent (IBD) shared by relatives. As a result, information about marker linkage phases in the parents is not required. The method has been studied extensively under either the maximum-likelihood framework or the sib-pair regression paradigm. However, virtually all investigations are limited to normally distributed traits under a single QTL model. In this study, we develop a Bayes method to map multiple QTL. We also extend the Bayesian mapping procedure to identify QTL responsible for the variation of complex binary diseases in humans under a threshold model. The method can also treat the number of QTL as a parameter and infer its posterior distribution. We use the reversible jump Markov chain Monte Carlo method to infer the posterior distributions of parameters of interest. The Bayesian mapping procedure ends with an estimation of the joint posterior distribution of the number of QTL and the locations and variances of the identified QTL. Utilities of the method are demonstrated using a simulated population consisting of multiple full-sib families.     

Testing the phenotypic gambit: phenotypic, genetic and environmental correlations of colour

Evolutionary theory is primarily concerned with genetic processes, yet empirical testing of this theory often involves data collected on phenotypes. To make this tenable, the implicit assumption is often made that phenotypic patterns are good predictors of genetic patterns; an assumption that coined the phenotypic gambit. Although this assumption has been validated for traits with high heritability, such as morphology, its generality for traits with low heritabilities, such as life-history and behavioural traits, remains controversial. Using a large-scale cross-fostering experiment, we were able to measure genetic, common environmental and phenotypic correlations between four colour traits and two skeletal traits in a wild population of passerine birds, the blue tit (Parus caeruleus). Colour traits had little heritable variation but common environment effects were found to be important; skeletal traits showed the opposite pattern. Positive correlations because of a shared natal environment were found between all traits, obscuring negative genetic correlations between some colour and skeletal traits. Consequently, phenotypic patterns were poor surrogates for genetic patterns and we suggest that this may be common if trade-offs or substantial parental effects exist. For this group of traits, the phenotypic gambit cannot be made and we suggest caution when inferring genetic patterns from phenotypic data, especially for behavioural and life-history traits.     

Evolution in changing environments: the "synthetic" work of Clausen, Keck, and Hiesey.

The studies of Clausen, Keck, and Hiesey (CKH) have been widely cited as exemplars of ecotypic differentiation in textbooks and in the primary literature. However, the scope of their findings and achievements is significantly greater than this. In this paper we analyze the research program of CKH, highlighting their major findings during the years when the modern synthesis of evolution was taking shape. That synthesis, curiously, drew little from their examples, although their studies at the Carnegie Institution represent conceptual and methodological work that is still relevant. The works of CKH not only embodied the principles of the nascent synthesis, but often provided needed supporting data. Their classic work, especially on Achillea and Potentilla, produced abundant evidence on population differentiation of many quantitative traits and plant phenotypes, as well as demonstrating the now commonly reported distinction between environmental and genetic determination of traits. Their ecological genetic investigations of quantitative traits in plants were in sharp contrast to contemporaneous animal studies on adaptation that focused on discrete polymorphisms--with correspondingly little influence of the environment on phenotypic expression. Of utmost importance was the demonstration by CKH of adaptive differentiation by natural selection and their approaches to understanding the genetic structure of populations.     

Genome-wide interaction of genotype by erythrocyte n-3 fatty acids contributes to phenotypic variance of diabetes-related traits

Background

Little is known about the interplay between n-3 fatty acids and genetic variants for diabetes-related traits at the genome-wide level. The present study aimed to examine variance contributions of genotype by environment (GxE) interactions for different erythrocyte n-3 fatty acids and genetic variants for diabetes-related traits at the genome-wide level in a non-Hispanic white population living in the U.S.A. (n = 820). A tool for Genome-wide Complex Trait Analysis (GCTA) was used to estimate the genome-wide GxE variance contribution of four diabetes-related traits: HOMA-Insulin Resistance (HOMA-IR), fasting plasma insulin, glucose and adiponectin. A GxE genome-wide association study (GWAS) was conducted to further elucidate the GCTA results. Replication was conducted in the participants of the Boston Puerto Rican Health Study (BPRHS) without diabetes (n = 716).

Results

In GOLDN, docosapentaenoic acid (DPA) contributed the most significant GxE variance to the total phenotypic variance of both HOMA-IR (26.5%, P-nominal = 0.034) and fasting insulin (24.3%, P-nominal = 0.042). The ratio of arachidonic acid to eicosapentaenoic acid + docosahexaenoic acid contributed the most significant GxE variance to the total variance of fasting glucose (27.0%, P-nominal = 0.023). GxE variance of the arachidonic acid/eicosapentaenoic acid ratio showed a marginally significant contribution to the adiponectin variance (16.0%, P-nominal = 0.058). None of the GCTA results were significant after Bonferroni correction (P < 0.001). For each trait, the GxE GWAS identified a far larger number of significant single-nucleotide polymorphisms (P-interaction ≤ 10E-5) for the significant E factor (significant GxE variance contributor) than a control E factor (non-significant GxE variance contributor). In the BPRHS, DPA contributed a marginally significant GxE variance to the phenotypic variance of HOMA-IR (12.9%, P-nominal = 0.068) and fasting insulin (18.0%, P-nominal = 0.033).

Conclusion

Erythrocyte n-3 fatty acids contributed a significant GxE variance to diabetes-related traits at the genome-wide level.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-15-781) contains supplementary material, which is available to authorized users.     

Linking the spatial scale of environmental variation and the evolution of phenotypic plasticity: selection favors adaptive plasticity in fine-grained environments

Adaptive phenotypic plasticity and adaptive genetic differentiation enable plant lineages to maximize their fitness in response to environmental heterogeneity. The spatial scale of environmental variation relative to the average dispersal distance of a species determines whether selection will favor plasticity, local adaptation, or an intermediate strategy. Habitats where the spatial scale of environmental variation is less than the dispersal distance of a species are fine grained and should favor the expression of adaptive plasticity, while coarse-grained habitats, where environmental variation occurs on spatial scales greater than dispersal, should favor adaptive genetic differentiation. However, there is relatively little information available characterizing the link between the spatial scale of environmental variation and patterns of selection on plasticity measured in the field. I examined patterns of spatial environmental variation within a serpentine mosaic grassland and selection on an annual plant (Erodium cicutarium) within that landscape. Results indicate that serpentine soil patches are a significantly finer-grained habitat than non-serpentine patches. Additionally, selection generally favored increased plasticity on serpentine soils and diminished plasticity on non-serpentine soils. This is the first empirical example of differential selection for phenotypic plasticity in the field as a result of strong differences in the grain of environmental heterogeneity within habitats.     

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.     

Species diversity improves the efficiency of mercury-reducing biofilms under changing environmental conditions

Six mercury-resistant environmental proteobacterial isolates and one genetically modified mercury-resistant Pseudomonas putida strain were analyzed for physiological traits of adaptive relevance in an environment of packed-bed bioreactors designed for the decontamination of mercury-polluted chlor-alkali wastewater. The strains displayed characteristic differences in each trait (i.e., biofilm formation capability, growth rate in mercury contaminated wastewaters, and mercury reduction efficiency). Subsequently, they were immobilized either as a monoculture or as a mixed culture on porous carrier material in packed-bed bioreactors through which different batches of filter-sterilized industrial chlor-alkali wastewater were pumped. In monospecies bioreactors, the mercury retention efficiency was sensitive to rapidly increasing mercury concentrations in the wastewater. Mixed culture biofilms displayed a high mercury retention efficiency that was not affected by rapid increases in mercury or continuously high mercury concentrations. The dynamic in the community composition of the mixed culture bioreactors was determined by ribosomal intergenic spacer polymorphism analysis. Mercury-mediated selective pressure decreased the number of prevalent strains. Microbial diversity was completely restored after easing of the selective pressure. Microbial diversity provides a reservoir of strains with complementary ecological niches that results in a superior bioreactor performance under changing environmental conditions.     

A quantitative model of the relationship between phenotypic variance and heterozygosity at marker loci under partial selfing.

Negative relationships between allozyme heterozygosity and morphological variance have often been observed and interpreted as evidence for increased developmental stability in heterozygotes. However, inbreeding can also generate such relationships by decreasing heterozygosity at neutral loci and redistributing genetic variance at the same time. I here provide a quantitative genetic model of this process by analogy with heterozygosity-fitness relationships. Inbreeding generates negative heterozygosity-variance relationships irrespective of the genetic architecture of the trait. This holds for fitness traits as well as neutral traits, the effect being stronger for fitness traits under directional dominance or overdominance. The order of magnitude of heterozygosity-variance regressions is compatible with empirical data even with very low inbreeding. Although developmental stability effects cannot be excluded, inbreeding is a parsimonious explanation that should be seriously considered to explain correlations between heterozygosity and both mean and variance of phenotypes in natural populations.     

Annual variations in the reproductive traits of Pomatoschistus microps in a Mediterranean lagoon undergoing environmental changes: evidence of phenotypic plasticity

The spawning period of the common goby Pomatoschistus microps from 1993 to 1997 in the Vaccarès lagoon did not vary, except in 1997 when it was longer due to the reproduction of the young-of-the-year. Egg size and number, and reproductive allocation varied greatly with one year to another. Female common gobies increased both their fecundity per spawning act and their egg size from 1993 to 1995. The annual variation in the reproductive effort suggests a high phenotypic plasticity of reproductive traits in P. microps , in the face of environmental perturbations. In winter 1993–1994, a centennial flood of the Rhône River caused major hydrological changes in the lagoon in less than 1 week, affecting many invertebrates and fish for several years. The reproductive investment of the common goby increased, possibly as a consequence of those environmental changes.