Effect of migration and environmental heterogeneity on the maintenance of quantitative genetic variation: a simulation study

The paradox of high genetic variation observed in traits under stabilizing selection is a long‐standing problem in evolutionary theory, as mutation rates appear too low to explain observed levels of standing genetic variation under classic models of mutation–selection balance. Spatially or temporally heterogeneous environments can maintain more standing genetic variation within populations than homogeneous environments, but it is unclear whether such conditions can resolve the above discrepancy between theory and observation. Here, we use individual‐based simulations to explore the effect of various types of environmental heterogeneity on the maintenance of genetic variation (V_A) for a quantitative trait under stabilizing selection. We find that V_A is maximized at intermediate migration rates in spatially heterogeneous environments and that the observed patterns are robust to changes in population size. Spatial environmental heterogeneity increased variation by as much as 10‐fold over mutation–selection balance alone, whereas pure temporal environmental heterogeneity increased variance by only 45% at max. Our results show that some combinations of spatial heterogeneity and migration can maintain considerably more variation than mutation–selection balance, potentially reconciling the discrepancy between theoretical predictions and empirical observations. However, given the narrow regions of parameter space required for this effect, this is unlikely to provide a general explanation for the maintenance of variation. Nonetheless, our results suggest that habitat fragmentation may affect the maintenance of V_A and thereby reduce the adaptive capacity of populations.     

Indirect genetic effects and the lek paradox: inter-genotypic competition may strengthen genotype × environment interactions and conserve genetic variance

Understanding the evolutionary mechanisms that maintain genetic variation in natural populations is one of the fundamental goals of evolutionary biology. There is growing evidence that genotype-by-environment interaction (G × E) can maintain additive genetic variance (V _A), but we lack information on the relative performance of genotypes under the competitive situations encountered in the field. Competing genotypes may influence each other, and this interaction is also subject to selection through indirect genetic effects (IGE). Here, we explore how genotypes perform when interacting and evaluate IGE in order to understand its influence on V _A for sexually-selected traits in the lesser waxmoth, Achroia grisella. We found that inter-genotype differences and crossover interactions under joint rearing are equal to or greater than values when reared separately. A focal genotype exhibited different performances when jointly reared with various genotypes—suggesting that IGE may be responsible for the increased levels of crossover and differences in performance observed. We suggest that some genotypes are superior competitors for food acquisition in the larval stage, and that these differences influence the development and evolution of other genotypes through IGE. We reaffirm the role of G × E in maintaining V _A and note the general importance of IGE in studies of evolutionary mechanisms.     

Genotype × environment interaction in the allometry of body,genitalia and signal traits in Enchenopa treehoppers (Hemiptera: Membracidae)

Developmental plasticity may promote divergence by exposing genetic variation to selection in novel ways in new environments. We tested for this effect in the static allometry (i.e. scaling on body size) of traits in advertisement signals, body and genitalia. We used a member of the Enchenopa binotata species complex of treehoppers – a clade of plant‐feeding insects in which speciation is associated with colonization of novel environments involving marked divergence in signals, subtle divergence in body size and shape, and no apparent divergence in genitalia. We found no change in mean allometric slopes across environments, but substantial genetic variation and genotype × environment interaction (G × E) in allometry. The allometry of signal traits showed the most genetic variation and G × E, and that of genitalia showed the weakest G × E. Our findings suggest that colonizing novel environments may have stronger diversifying consequences for signal allometry than for genitalia allometry. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 187–196.     

Heritability and evolvability of fitness and nonfitness traits: Lessons from livestock

Data from natural populations have suggested a disconnection between trait heritability (variance standardized additive genetic variance, V_A) and evolvability (mean standardized V_A) and emphasized the importance of environmental variation as a determinant of trait heritability but not evolvability. However, these inferences are based on heterogeneous and often small datasets across species from different environments. We surveyed the relationship between evolvability and heritability in >100 traits in farmed cattle, taking advantage of large sample sizes and consistent genetic approaches. Heritability and evolvability estimates were positively correlated (r = 0.37/0.54 on untransformed/log scales) reflecting a substantial impact of V_A on both measures. Furthermore, heritabilities and residual variances were uncorrelated. The differences between this and previously described patterns may reflect lower environmental variation experienced in farmed systems, but also low and heterogeneous quality of data from natural populations. Similar to studies on wild populations, heritabilities for life‐history and behavioral traits were lower than for other traits. Traits having extremely low heritabilities and evolvabilities (17% of the studied traits) were almost exclusively life‐history or behavioral traits, suggesting that evolutionary constraints stemming from lack of genetic variability are likely to be most common for classical “fitness” (cf. life‐history) rather than for “nonfitness” (cf. morphological) traits.     

Population size is weakly related to quantitative genetic variation and trait differentiation in a stream fish

How population size influences quantitative genetic variation and differentiation among natural, fragmented populations remains unresolved. Small, isolated populations might occupy poor quality habitats and lose genetic variation more rapidly due to genetic drift than large populations. Genetic drift might furthermore overcome selection as population size decreases. Collectively, this might result in directional changes in additive genetic variation (V_A) and trait differentiation (Q_ST) from small to large population size. Alternatively, small populations might exhibit larger variation in V_A and Q_ST if habitat fragmentation increases variability in habitat types. We explored these alternatives by investigating V_A and Q_ST using nine fragmented populations of brook trout varying 50‐fold in census size N (179–8416) and 10‐fold in effective number of breeders, N_b (18–135). Across 15 traits, no evidence was found for consistent differences in V_A and Q_ST with population size and almost no evidence for increased variability of V_A or Q_ST estimates at small population size. This suggests that (i) small populations of some species may retain adaptive potential according to commonly adopted quantitative genetic measures and (ii) populations of varying sizes experience a variety of environmental conditions in nature, however extremely large studies are likely required before any firm conclusions can be made.     

The role of ecology,neutral processes and antagonistic coevolution in an apparent sexual arms race

Some of the strongest examples of a sexual ‘arms race’ come from observations of correlated evolution in sexually antagonistic traits among populations. However, it remains unclear whether these cases truly represent sexually antagonistic coevolution; alternatively, ecological or neutral processes might also drive correlated evolution. To investigate these alternatives, we evaluated the contributions of intersex genetic correlations, ecological context, neutral genetic divergence and sexual coevolution in the correlated evolution of antagonistic traits among populations of Gerris incognitus water striders. We could not detect intersex genetic correlations for these sexually antagonistic traits. Ecological variation was related to population variation in the key female antagonistic trait (spine length, a defence against males), as well as body size. Nevertheless, population covariation between sexually antagonistic traits remained substantial and significant even after accounting for all of these processes. Our results therefore provide strong evidence for a contemporary sexual arms race.     

Genetic variance in fitness and its cross-sex covariance predict adaptation during experimental evolution

The additive genetic variation (V_A) of fitness in a population is of particular importance to quantify its adaptive potential and predict its response to rapid environmental change. Recent statistical advances in quantitative genetics and the use of new molecular tools have fostered great interest in estimating fitness V_A in wild populations. However, the value of V_A for fitness in predicting evolutionary changes over several generations remains mostly unknown. In our study, we addressed this question by combining classical quantitative genetics with experimental evolution in the model organism Tribolium castaneum (red flour beetle) in three new environmental conditions (Dry, Hot, Hot-Dry). We tested for potential constraints that might limit adaptation, including environmental and sex genetic antagonisms captured by negative genetic covariance between environments and female and male fitness, respectively. Observed fitness changes after 20 generations mainly matched our predictions. Given that body size is commonly used as a proxy for fitness, we also tested how this trait and its genetic variance (including nonadditive genetic variance) were impacted by environmental stress. In both traits, genetic variances were sex and condition dependent, but they differed in their variance composition, cross-sex and cross-environment genetic covariances, as well as in the environmental impact on V_A.     

Experimental evolution for generalists and specialists reveals multivariate genetic constraints on thermal reaction norms

Theory predicts the emergence of generalists in variable environments and antagonistic pleiotropy to favour specialists in constant environments, but empirical data seldom support such generalist–specialist trade‐offs. We selected for generalists and specialists in the dung fly Sepsis punctum (Diptera: Sepsidae) under conditions that we predicted would reveal antagonistic pleiotropy and multivariate trade‐offs underlying thermal reaction norms for juvenile development. We performed replicated laboratory evolution using four treatments: adaptation at a hot (31 °C) or a cold (15 °C) temperature, or under regimes fluctuating between these temperatures, either within or between generations. After 20 generations, we assessed parental effects and genetic responses of thermal reaction norms for three correlated life‐history traits: size at maturity, juvenile growth rate and juvenile survival. We find evidence for antagonistic pleiotropy for performance at hot and cold temperatures, and a temperature‐mediated trade‐off between juvenile survival and size at maturity, suggesting that trade‐offs associated with environmental tolerance can arise via intensified evolutionary compromises between genetically correlated traits. However, despite this antagonistic pleiotropy, we found no support for the evolution of increased thermal tolerance breadth at the expense of reduced maximal performance, suggesting low genetic variance in the generalist–specialist dimension.     

Genic capture and the genetic basis of sexually selected traits in the zebra finch

Abstract The lek paradox, in which female choice erodes genetic variation in male sexually selected traits, is a fundamental issue in sexual selection. If females gain only genetic benefits from preferentially having their ova fertilized by males with particular traits, what maintains variation in these traits? Under strong directional selection mediated through mate choice, the alleles for beneficial male traits are expected to go to fixation and exhibit little variation. A theoretical solution to the lek paradox is the genic capture hypothesis which states that: costly male traits subject to female choice are condition dependent, that male condition is dependent on genes at many loci and exhibits additive genetic variance, and that positive genetic correlations exist between sexually selected traits and condition. Using a captive population of the zebra finch Taeniopygia guttata, we tested two key predictions from this model: (1) that genetic variance exists in beak color which is a sexually selected trait, but also in condition and immune function, and (2) that positive genetic correlations exist between condition and beak color, and between beak color, condition, and immune function. Genetic parameters were estimated from a large breeding experiment involving 81 sires, 972 offspring, a pedigree of 1526 individuals, using the animal model. We employed the following index of body condition: residuals from a log‐log plot of body mass on tarsus length following a standardized and extended period of exercise, in which residual mass is known to reflect fat and protein reserves. Our results were broadly consistent with the genic capture hypothesis because we found (1) additive genetic variation in beak color and immune function and condition, and (2) positive genetic correlations between condition and beak color, and between condition, beak color, and several assays of immune responsiveness. However, both of these results need qualification. In the first case we identified an important general problem in estimating the coefficient of additive genetic variance (CV_A) in body condition. In the second case, although most of the genetic correlations were positive as predicted, only some were statistically significant, possibly due to our relatively small sample sizes, because genetic correlations typically have large standard errors and therefore require very large samples to be statistically significant. The statistically significant, positive genetic correlations included those between beak color and immune function (response to tetanus), and between immune function (response to tetanus) and condition, both of which indicate that females gain good genes from mating with males in good condition and/or with a redder beak color. We discuss the implications of our results for devising more rigorous but pragmatic tests of the genic capture hypothesis.     

Does natural selection alter genetic architecture? An evaluation of quantitative genetic variation among populations of Allonemobiussocius and A. fasciatus

To make long-term predictions using present quantitative genetic theory it is necessary to assume that the genetic variance–covariance matrix ( G ) remains constant or at least changes by a constant fraction. In this paper we examine the stability of the genetic architecture of two traits known to be subject to natural selection; femur length and ovipositor length in two species of the cricket Allonemobius. Previous studies have shown that in A. fasciatus and A. socius natural selection favours an increased body size southwards but a decreased ovipositor length. Such countergradient selection should tend to favour a change in G . In the total sample of eight populations of A. socius and one of A. fasciatus we show that there is significant variation in all genetic covariance components, i.e. V_A for body size, V_A for ovipositor length, and Cov_A. This variation results entirely from an increase in the covariances of A. fasciatus. However, although larger, these components are approximately proportionally increased, thereby leading to no statistically significant change in the genetic correlation. A proportional increase in the covariance components is consistent with changes resulting from genetic drift. On the other hand, the genetic covariance components are significantly correlated with the length of the growing season suggesting that the change in the genetic architecture is the result of selection and drift.     

Spatially and temporally varying selection on intrapopulation quantitative trait loci for a life history trade-off in Mimulus guttatus

Why do populations remain genetically variable despite strong continuous natural selection? Mutation reconstitutes variation eliminated by selection and genetic drift, but theoretical and experimental studies each suggest that mutation‐selection balance insufficient to explain extant genetic variation in most complex traits. The alternative hypothesis of balancing selection, wherein selection maintains genetic variation, is an aggregate of multiple mechanisms (spatial and temporal heterogeneity in selection, frequency‐dependent selection, antagonistic pleiotropy, etc.). Most of these mechanisms have been demonstrated for Mendelian traits, but there is little comparable data for loci affecting quantitative characters. Here, we report a 3‐year field study of selection on intrapopulation quantitative trait loci (QTL) of flower size, a highly polygenic trait in Mimulus guttatus. The QTL exhibit antagonistic pleiotropy: alleles that increase flower size, reduce viability, but increase fecundity. The magnitude and direction of selection fluctuates yearly and on a spatial scale of metres. This study provides direct evidence of balancing selection mechanisms on QTL of an ecologically relevant trait.     

Genetic by environment interactions affect plant–soil linkages

The role of plant intraspecific variation in plant–soil linkages is poorly understood, especially in the context of natural environmental variation, but has important implications in evolutionary ecology. We utilized three 18‐ to 21‐year‐old common gardens across an elevational gradient, planted with replicates of five Populus angustifolia genotypes each, to address the hypothesis that tree genotype (G), environment (E), and G × E interactions would affect soil carbon and nitrogen dynamics beneath individual trees. We found that soil nitrogen and carbon varied by over 50% and 62%, respectively, across all common garden environments. We found that plant leaf litter (but not root) traits vary by genotype and environment while soil nutrient pools demonstrated genotype, environment, and sometimes G × E interactions, while process rates (net N mineralization and net nitrification) demonstrated G × E interactions. Plasticity in tree growth and litter chemistry was significantly related to the variation in soil nutrient pools and processes across environments, reflecting tight plant–soil linkages. These data overall suggest that plant genetic variation can have differential affects on carbon storage and nitrogen cycling, with implications for understanding the role of genetic variation in plant–soil feedback as well as management plans for conservation and restoration of forest habitats with a changing climate.     

Environmental heterogeneity generates opposite gene‐by‐environment interactions for two fitness‐related traits within a population

Theory predicts that environmental heterogeneity offers a potential solution to the maintenance of genetic variation within populations, but empirical evidence remains sparse. The live‐bearing fish Xiphophorus variatus exhibits polymorphism at a single locus, with different alleles resulting in up to five distinct melanistic “tailspot” patterns within populations. We investigated the effects of heterogeneity in two ubiquitous environmental variables (temperature and food availability) on two fitness‐related traits (upper thermal limits and body condition) in two different tailspot types (wild‐type and upper cut crescent). We found gene‐by‐environment (G × E) interactions between tailspot type and food level affecting upper thermal limits (UTL), as well as between tailspot type and thermal environment affecting body condition. Exploring mechanistic bases underlying these G × E patterns, we found no differences between tailspot types in hsp70 gene expression despite significant overall increases in expression under both thermal and food stress. Similarly, there was no difference in routine metabolic rates between the tailspot types. The reversal of relative performance of the two tailspot types under different environmental conditions revealed a mechanism by which environmental heterogeneity can balance polymorphism within populations through selection on different fitness‐related traits.     

Comparing the intersex genetic correlation for fitness across novel environments in the fruit fly,Drosophila serrata

Sexually antagonistic genetic variation can pose limits to the independent evolution and adaptation of the sexes. The extent of sexually antagonistic variation is reflected in the intersex genetic correlation for fitness (r_w^FM). Previous estimates of this correlation have been mostly limited to populations in environments to which they are already well adapted, making it difficult to gauge the importance of sexually antagonistic genetic variance during the early stages of adaptation, such as that occurring following abrupt environmental change or upon the colonization of new habitat. Here we assayed male and female lifetime fitness in a population of Drosophila serrata in four novel laboratory environments. We found that r_w^FM varied significantly across environments, with point estimates ranging from positive to negative values of considerable magnitude. We also found that the variability among estimates was because, at least in part, of significant differences among environments in the genetic variances of both male and female fitness, with no evidence of any significant changes in the intersex covariance itself, although standard errors of these estimates were large. Our results illustrate the unpredictable nature of r_w^FM in novel environments and suggest that, although sexually antagonistic genetic variance can be pronounced in some novel environments, it may have little effect in constraining the early stages of adaptation in others.     

Selection mosaics differentiate Rhizobium–host plant interactions across different nitrogen environments

The nature and direction of coevolutionary interactions between species is expected to differentiate among distinct environments. Consequently, locally coevolved symbiotic traits would be well matched in similar environments, but mismatched elsewhere. In a classic mutualistic tradeoff, rhizobia provide nitrogen (N) to legume host plants in return for photosynthates. Despite earlier predictions, there is little evidence so far that spatial differences in soil N content mediate the coevolutionary outcome of the legume–Rhizobium mutualism. To test the existence of such selection mosaics, different genotypes of Vicia cracca and Rhizobium leguminosarum originating from spatially and environmentally highly differentiated sites were cross inoculated across different soil N regimes. In accordance with theoretical predictions, we found highly significant effects of genotype by genotype by environment (G× G × E) interactions, on both nodulation and plant growth, even when R. leguminosarum genotypes showed high genetic similarity. Our results show that the trajectory of the coevolutionary interactions between rhizobia and legumes is differentiated across different environments, and that selection mosaics may play an important role in shaping differences in the genetic composition of rhizobial populations.     

Effects of temperature extremes on genetic variances for life history traits in Drosophila melanogaster as determined from parent-offspring comparisons

Parent-offspring comparisons were used to investigate the effects of temperature extremes on genetic variances for two life history traits and one morphological trait in Drosophila melanogaster. We considered three temperatures (14 °C, 25 °C and 28 °C) for culturing and testing flies, and considered heritabilities, coefficients of additive variation (CV_A) and evolvabilities (I_A) for fecundity, development time and wing length. For fecundity, heritabilities and evolvabilities were higher when parents were exposed to 14 °C compared to 28 °C. Parent-offspring comparisons suggested that genetic correlations among environments were close to 1, although lower correlations were obtained in comparisons of family means. Parent-offspring correlations across environments seemed to depend on parental temperature. For development time, heritabilities and evolvabilities were low at 14 °C compared to 28 °C. However, parent-offspring correlations were relatively high when the progeny of parents tested at 14 °C were raised at the opposite extreme, suggesting that genetic variation can be enhanced when parents and offspring experience different conditions. CV_As and I_As for development time were lower than for fecundity, even when heritability estimates were similar in magnitude. Genetic variation for wing length was generally not affected by the temperature extremes, and genetic correlations across the extremes estimated from the parent-offspring comparison were close to 1. There was no evidence for tradeoffs between traits; rapid development time was associated with high fecundity at both the phenotypic and genetic levels. The findings highlight inherent difficulties of estimating genetic parameters from parent-offspring comparisons when two generations experience different environmental extremes and also show how parent-offspring comparisons can lead to unexpected findings about the expression of genetic variation.     

The effect of trait type and strength of selection on heritability and evolvability in an island bird population

The heritability (h²) of fitness traits is often low. Although this has been attributed to directional selection having eroded genetic variation in direct proportion to the strength of selection, heritability does not necessarily reflect a trait's additive genetic variance and evolutionary potential (“evolvability”). Recent studies suggest that the low h² of fitness traits in wild populations is caused not by a paucity of additive genetic variance (V_A) but by greater environmental or nonadditive genetic variance (V_R). We examined the relationship between h² and variance‐standardized selection intensities (i or β_σ), and between evolvability (I_A:V_A divided by squared phenotypic trait mean) and mean‐standardized selection gradients (β_μ). Using 24 years of data from an island population of Savannah sparrows, we show that, across diverse traits, h² declines with the strength of selection, whereas I_A and I_R (V_R divided by squared trait mean) are independent of the strength of selection. Within trait types (morphological, reproductive, life‐history), h², I_A, and I_R are all independent of the strength of selection. This indicates that certain traits have low heritability because of increased residual variance due to the age at which they are expressed or the multiple factors influencing their expression, rather than their association with fitness.     

Sexual antagonism for resistance and tolerance to infection in Drosophila melanogaster

A critical task in evolutionary genetics is to explain the persistence of heritable variation in fitness-related traits such as immunity. Ecological factors can maintain genetic variation in immunity, but less is known about the role of other factors, such as antagonistic pleiotropy, on immunity. Sexually dimorphic immunity—with females often being more immune-competent—may maintain variation in immunity in dioecious populations. Most eco-immunological studies assess host resistance to parasites rather than the host''s ability to maintain fitness during infection (tolerance). Distinguishing between resistance and tolerance is important as they are thought to have markedly different evolutionary and epidemiological outcomes. Few studies have investigated tolerance in animals, and the extent of sexual dimorphism in tolerance is unknown. Using males and females from 50 Drosophila melanogaster genotypes, we investigated possible sources of genetic variation for immunity by assessing both resistance and tolerance to the common bacterial pathogen Pseudomonas aeruginosa. We found evidence of sexual dimorphism and sexual antagonism for resistance and tolerance, and a trade-off between the two traits. Our findings suggest that antagonistic pleiotropy may be a major contributor to variation in immunity, with implications for host–parasite coevolution.