Climate change shifts natural selection and the adaptive potential of the perennial forb Boechera stricta in the Rocky Mountains

Heritable genetic variation is necessary for populations to evolve in response to anthropogenic climate change. However, antagonistic genetic correlations among traits may constrain the rate of adaptation, even if substantial genetic variation exists. We examine potential genetic responses to selection by comparing multivariate genetic variance–covariances of traits and fitness (multivariate Robertson–Price identities) across different environments in a reciprocal transplant experiment of the forb Boechera stricta in the Rocky Mountains. By transplanting populations into four common gardens arrayed along an elevational gradient, and exposing populations to control and snow removal treatments, we simulated future and current climates and snowmelt regimes. Genetic variation in flowering and germination phenology declined in plants moved downslope to warmer, drier sites, suggesting that these traits may have a limited ability to evolve under future climates. Simulated climate change via snow removal altered the strength of selection on flowering traits, but we found little evidence that genetic correlations among traits are likely to affect the rate of adaptation to climate change. Overall, our results suggest that climate change may alter the evolutionary potential of B. stricta, but reduced expression of genetic variation may be a larger impediment to adaptation than constraints imposed by antagonistic genetic correlations.     

A search for trade-offs among life history traits inDrosophila melanogaster

Summary Are there underlying developmental and physiological properties of organisms that can be used to build a general theory of life history evolution? Much of the theoretical work on the evolution of life histories is based on the premise of negative developmental and genetic correlations among life history traits. If negative correlations do not exist as a general rule then no general theory taking them into account is possible. Negative genetic correlations among life history traits can come about by antagonistic pleiotropy. One cause of antagonistic pleiotropy is cost allocation trade-offs. Since cost allocation trade-offs are due to underlying physiological constraints they are expected to be common to closely related groups. A second form of antagonistic pleiotropy is specialization of genotypes to different niches. This type of antagonistic pleiotropy is expected to be specific to each population. We looked for trade-offs in life history traits of longevity and fecundity inDrosophila melanogaster. We used a half-sib mating design and raised the offspring at two temperatures, 19°C and 25°C. Correlations between longevity and fecundity showed some evidence of antagonistic pleiotropy at high temperature with no evidence of any trade-offs at low temperature. Correlations of early and late fecundity traits did show evidence of cost allocation trade-offs at both temperatures. Antagonistic pleiotropy was also found for cross-environmental correlations of fecundity traits. We conclude that, although life history trade-offs can not be generally assumed, they are frequently found among functionally related traits. Thus, we provide guidelines for the development of general theories of life history evolution.     

QUANTITATIVE GENETICS OF SURVIVAL AND GROWTH IN IMPATIENS CAPENSIS

When variation in life-history characters is caused by many genes of small effect, then quantitative-genetic parameters may quantify constraints on rate and direction of microevolutionary change. I estimated heritabilities and genetic correlations for 16 life-history and morphological characters in two populations of Impatiens capensis, a partially self-pollinating herbaceous annual. The Madison population had little or no additive genetic variance for any of these characters, while the Milwaukee population had significant narrowsense heritabilities and genetic correlations for several traits, including adult size, which is highly correlated with fitness. All genetic correlations among fitness components were positive, hence there is no evidence for antagonistic pleiotropy among these traits. Dissimilarity of heritabilities in the two populations supports theoretical predictions that long-term changes in genetic variance-covariance patterns may occur when population sizes are small and selection is strong, as may occur in many plant species.     

Evolution of drought tolerance and defense: dependence of tradeoffs on mechanism, environment and defense switching

Plants evolve defenses against herbivores and pathogens in stressful environments; however, plants that evolve tolerances to other environmental stressors may have compromised defenses. Such tradeoffs involving defenses may depend on limited resources or otherwise stressful environments; however, the effect of stressful environments on defense expression might be different for different genotypes (G×E). To test these predictions, we studied genetic variation and co‐variation of drought stress tolerance and defenses at two levels of genetic variation: between and within closely related species. We did this across an experimental drought stress gradient in a growth room for species for which genetic variation in drought tolerance was likely. In apparent contrast to predictions, the species Boechera holboellii (Brassicaceae) from lower and dryer elevations had slower inherent growth rates and correspondingly higher total defensive glucosinolate concentrations than the closely related species B. stricta from higher elevations. Thus, B. holboellii was both drought tolerant and defended; however, optimality theory does predict tradeoffs between defense and growth. Differences between species in the direct effect of water deficiency on glucosinolate production did not obscure the grow‐or‐defend tradeoff. B. holboellii may also have been more resistant to the specialist herbivore Plutella xylostella; a trend that was less clear because it depended on plant development and water deficient conditions. At finer scales of genetic variation, there was significant variation among families and naturally occurring inbred lines of B. stricta in drought tolerance measured as inherent growth, the reaction norm of growth across drought treatments, shoot water potential, and transpiration rates. Evidence for tradeoffs was also found within B. stricta in genetic correlations between resistance and transpiration rates, or glucosinolates and growth rates. No G×E was detected at these finer scales of genetic variation, although sometimes the tradeoff was dependent on drought conditions. Direct effects of drought stress resulted in an apparent plastic switch between resistance and tolerance to damage, which might be a cost avoidance mechanism because tradeoffs never involved tolerance to damage. Thus, when drought tolerance is manifest as slow inherent growth rates, plants may also have relatively high defense levels, especially in stressful environments. Otherwise, defenses may be compromised by drought‐coping mechanisms, although plastic switches to less costly defenses may alleviate constraints in stressful environments.     

Genetic dissection of adaptive form and function in rapidly speciating cichlid fishes

Genes of major phenotypic effects and strong genetic correlations can facilitate adaptation, direct selective responses, and potentially lead to phenotypic convergence. However, the preponderance of this type of genetic architecture in repeatedly evolved adaptations remains unknown. Using hybrids between Haplochromis chilotes (thick‐lipped) and Pundamilia nyererei (thin‐lipped) we investigated the genetics underlying hypertrophied lips and elongated heads, traits that evolved repeatedly in cichlids. At least 25 loci of small‐to‐moderate and mainly additive effects were detected. Phenotypic variation in lip and head morphology was largely independent. Although several QTL overlapped for lip and head morphology traits, they were often of opposite effects. The distribution of effect signs suggests strong selection on lips. The fitness implications of several detected loci were demonstrated using a laboratory assay testing for the association between genotype and variation in foraging performance. The persistence of low fitness alleles in head morphology appears to be maintained through antagonistic pleiotropy/close linkage with positive‐effect lip morphology alleles. Rather than being based on few major loci with strong positive genetic correlations, our results indicate that the evolution of the Lake Victoria thick‐lipped ecomorph is the result of selection on numerous loci distributed throughout the genome.     

GENETIC CONSTRAINTS TO LIFE-HISTORY EVOLUTION IN THE PITCHER-PLANT MOSQUITO,WYEOMYIA SMITHII

Life-history theory relies heavily on the hypothesis that genetic tradeoffs among the components of fitness constrain their independent evolution and joint maximization. Herein we show that selection on preadult development time in the pitcher-plant mosquito, Wyeomyia smithii, leads to a correlated response in cohort mean generation time but no correlated response in survivorship, fecundity, or cohort replacement rate. Lines selected for fast development achieve a higher capacity for increase (r_c) than lines selected for slow development, independently of larval density. These results imply that tradeoffs due to underlying antagonistic pleiotropy affecting growth, development, survivorship, and reproduction are not necessary constraints to life-history evolution. Previous work with W. smithii has shown a positive genetic correlation between development time and a general, genetically coordinated diapause syndrome. We propose that the observed nontradeoffs among the components of r_c may be subsumed into an even more fundamental tradeoff between performance during the summer generations and synchronization of development and reproduction with the changing seasons. Consequently, critical tests of genetic tradeoffs as a constraint to the independent evolution or simultaneous optimization of fitness components may need to consider the seasonal context.     

High herbivore pressure favors constitutive over induced defense

Theoretical and empirical studies show that, when past or current herbivory is a reliable cue of future attack and defenses are costly, defenses can be induced only when needed and thereby permit investment in other functions such as growth or reproduction. Theory also states that, in environments where herbivory is constantly high, constitutive defenses should be favored. Here, we present data to support the second aspect of the induced resistance hypothesis. We examined herbivore‐induced responses for four species of Inga (Fabaceae), a common canopy tree in Neotropical forests. We quantified chemical defenses of expanding leaves, including phenolic, saponin and toxic amino acids, in experimental field treatments with and without caterpillars. Because young leaves lack fiber and are higher in protein than mature leaves, they typically lose >25% of their leaf area during the few weeks of expansion. We predicted that the high rates of attack would select for investment in constitutive defenses over induction. Our data show that chemical defenses were quite unresponsive to herbivory. We demonstrated that expanding leaves showed no or only small increases in investment in secondary metabolites, and no qualitative changes in the phenolic compound profile in response to herbivory. The proteinogenic amino acid tyrosine, which can be toxic at high concentrations, showed the greatest levels of induction. Synthesis: These results provide some of the first support for theoretical predictions that the evolution of induced vs. constitutive defenses depends on the risk of herbivory. In habitats with constant and high potential losses to herbivores, such as tropical rainforests, high investments in constitutive defenses are favored over induction.     

Contrasting mechanisms of secondary metabolite accumulation during leaf development in two tropical tree species with different leaf expansion strategies

Young leaves of most species experience remarkably higher herbivore attack rates than mature leaves. Considerable theoretical effort has focused on predicting optimal defense and tradeoffs in defense allocation during leaf expansion. Among others, allocation to secondary chemistry may be dependent on growth constraints. We studied flavanoid production during leaf development in two species of Inga (Fabaceae: Mimosoideae) with different expansion strategies: Inga goldmanii, a species with slowly expanding young leaves, and Inga umbellifera, a species with fast-expanding young leaves. In these two species, the most abundant and toxic class of defensive compounds is flavanoids (which include tannins). We measured their concentration by leaf dry weight, their total content per leaf, their HPLC chemical profile and their toxicity to a generalist herbivore at different expansion levels. Although in both species the flavanoid concentration decreased with increasing leaf expansion, that decrease was twice as pronounced for I. umbellifera as it was for I. goldmanii. I. umbellifera leaves produced flavanoids only during the first half of their development while I. goldmanii leaves continued production throughout. The changes in flavanoid HPLC profiles and toxicity were also more dramatic for I. umbellifera, which had different flavanoids in young than in mature leaves. Relative to I. umbellifera, I. goldmanii showed smaller changes in both flavanoid composition and toxicity in the transition from young to mature leaves. These results indicate that, even though young leaves suffer higher rates of attack and are predicted to have better chemical defenses than mature leaves, growth constraints may modulate defense allocation and thus, evolution of defense strategies.Electronic Supplementary Material Supplementary material is available for this article at and is accessible for authorized users.     

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.     

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.     

ANALYSIS OF THE GENETIC STRUCTURE OF LIFE HISTORY OF DROSOPHILA MELANOGASTER USING RECOMBINANT EXTRACTED LINES

A model for the evolution of senescence known as “antagonistic pleiotropy” makes the specific prediction that there should be a negative genetic correlation between early- and late-age traits associated with fitness. This model has previously been tested by classical quantitative-genetic means including sib-analysis and artificial selection. We used the approach of chromosome extraction, which has both advantages and disadvantages compared to classical techniques, to test the model further. From four isogenic lines of Drosophila melanogaster, four sets of recombinant extracted lines were constructed using standard balancer-chromosome techniques. The four parental lines and 53 recombinants were reared under controlled laboratory conditions and isolated as pairs for scoring daily fecundity and longevity. Even though the design is not optimal for estimating classical components of genetic variance, it afforded a uniquely direct test of the magnitude of environmental covariances, while giving a detailed genetic picture of part of the genome. There were clear differences among the recombinant series in the distribution of mean longevity and early fecundity. The genetic correlation between early fecundity (sum of egg production for the first five days posteclosion) and female longevity was significantly negative in only one of the recombinant series. When all lines were considered together, the phenotypic correlation between these traits was significantly negative (P < 0.02), while the broad-sense genetic correlation was –0.219 (P < 0.11). This result may be viewed as weakly consistent with the model of antagonistic pleiotropy, but other aspects of the data are at odds with the model.     

What affects the predictability of evolutionary constraints using a G‐matrix? The relative effects of modular pleiotropy and mutational correlation

Phenotypic traits do not always respond to selection independently from each other and often show correlated responses to selection. The structure of a genotype‐phenotype map (GP map) determines trait covariation, which involves variation in the degree and strength of the pleiotropic effects of the underlying genes. It is still unclear, and debated, how much of that structure can be deduced from variational properties of quantitative traits that are inferred from their genetic (co) variance matrix ( G ‐matrix). Here we aim to clarify how the extent of pleiotropy and the correlation among the pleiotropic effects of mutations differentially affect the structure of a G ‐matrix and our ability to detect genetic constraints from its eigen decomposition. We show that the eigenvectors of a G ‐matrix can be predictive of evolutionary constraints when they map to underlying pleiotropic modules with correlated mutational effects. Without mutational correlation, evolutionary constraints caused by the fitness costs associated with increased pleiotropy are harder to infer from evolutionary metrics based on a G ‐matrix's geometric properties because uncorrelated pleiotropic effects do not affect traits' genetic correlations. Correlational selection induces much weaker modular partitioning of traits' genetic correlations in absence then in presence of underlying modular pleiotropy.     

Compartmentalization of specialized metabolites across vegetative and reproductive tissues in two sympatric Psychotria species

Premise

The specialized metabolites of plants are recognized as key chemical traits in mediating the ecology and evolution of sundry plant–biotic interactions, from pollination to seed predation. Intra- and interspecific patterns of specialized metabolite diversity have been studied extensively in leaves, but the diverse biotic interactions that contribute to specialized metabolite diversity encompass all plant organs. Focusing on two species of Psychotria shrubs, we investigated and compared patterns of specialized metabolite diversity in leaves and fruit with respect to each organ's diversity of biotic interactions.

Methods

To evaluate associations between biotic interaction diversity and specialized metabolite diversity, we combined UPLC-MS metabolomic analysis of foliar and fruit specialized metabolites with existing surveys of leaf- and fruit-centered biotic interactions. We compared patterns of specialized metabolite richness and variance among vegetative and reproductive tissues, among plants, and between species.

Results

In our study system, leaves interact with a far larger number of consumer species than do fruit, while fruit-centric interactions are more ecologically diverse in that they involve antagonistic and mutualistic consumers. This aspect of fruit-centric interactions was reflected in specialized metabolite richness—leaves contained more than fruit, while each organ contained over 200 organ-specific specialized metabolites. Within each species, leaf- and fruit-specialized metabolite composition varied independently of one another across individual plants. Contrasts in specialized metabolite composition were stronger between organs than between species.

Conclusions

As ecologically disparate plant organs with organ-specific specialized metabolite traits, leaves and fruit can each contribute to the tremendous overall diversity of plant specialized metabolites.     

Multivariate selection under adverse genetic correlations: impacts of population sizes and selection strategies on gains and coancestry in forest tree breeding

We examined gene models for two traits with and without antagonistic pleiotropy using a locus-based simulation model to investigate the effects of different population sizes, heritabilities and economic weights, using index selection, and index selection with optimum selection (OS), over 10 generations. Gene models included additive and dominance gene action, with equal and varying initial allele frequencies with and without pleiotropy for a fixed level of resources (i.e. founder sizes each generation of 40, 80 and 160 with progeny arrays that totaled 800 per generation). Pleiotropy (with an initial r _g of −0.5), reduced gain by ~8–10% when heritabilities for both traits were the same (0.2), relative to non-pleiotropic cases. When traits had different heritabilities (i.e. 0.2 and 0.4), gains in the lower heritability trait were substantially lower, especially with pleiotropy present. In general, OS with slightly larger population sizes could offset losses in gain, but rarely overrode the large effects of different heritabilities or economic weights. Pleiotropy increased response variance among traits, which was magnified when heritabilities were different. Identifying an appropriate weight on relatedness in the OS process is important to manage coancestry expectations around the loss of alleles (or fixation of recessive alleles) and to minimise response variance. The dynamics of selection intensity, drift, rate of coancestry build-up, response variance, etc. are complex for multi-trait selection; however, a few economically viable strategies could reduce the adverse effects of selecting against genetic correlations without drastically impairing gain.     

Rapid independent trait evolution despite a strong pleiotropic genetic correlation

Genetic correlations are the most commonly studied of all potential constraints on adaptive evolution. We present a comprehensive test of constraints caused by genetic correlation, comparing empirical results to predictions from theory. The additive genetic correlation between the filament and the corolla tube in wild radish flowers is very high in magnitude, is estimated with good precision (0.85 ± 0.06), and is caused by pleiotropy. Thus, evolutionary changes in the relative lengths of these two traits should be constrained. Still, artificial selection produced rapid evolution of these traits in opposite directions, so that in one replicate relative to controls, the difference between them increased by six standard deviations in only nine generations. This would result in a 54% increase in relative fitness on the basis of a previous estimate of natural selection in this population, and it would produce the phenotypes found in the most extreme species in the family Brassicaceae in less than 100 generations. These responses were within theoretical expectations and were much slower than if the genetic correlation was zero; thus, there was evidence for constraint. These results, coupled with comparable results from other species, show that evolution can be rapid despite the constraints caused by genetic correlations.     

Evolutionary mechanisms of senescence

This paper reviews theories of the evolution of senescence. The population genetic basis for the decline with age in sensitivity of fitness to changes in survival and fecundity is discussed. It is shown that this creates a presure of selection that disproportionately favors performance early in life. The extent of this bias is greater when there is a high level of extrinsic mortality; this accounts for much the diversity in life-history patterns among different taxa. The implications of quantitative genetic theory for experimental tests of alternative population genetic models of senescence are discussed. In particular, the negative genetic correlations between traits predicted by the antagonistic pleiotropy model may be obscured by positive correlations that are inevitable in a multivariate system, or by the effects of variation due to deleterious mutations. The status of the genetic evidence relevant to these theories is discussed.     

Trade-off between age of first reproduction and survival in a female primate

Trade-offs are central to life-history theory but difficult to document. Patterns of phenotypic and genetic correlations in rhesus macaques, Macaca mulatta—a long-lived, slow-reproducing primate—are used to test for a trade-off between female age of first reproduction and adult survival. A strong positive genetic correlation indicates that female macaques suffer reduced adult survival when they mature relatively early and implies primate senescence can be explained, in part, by antagonistic pleiotropy. Contrasts with a similar human study implicate the extension of parental effects to later ages as a potential mechanism for circumventing female life-history trade-offs in human evolution.     

MULTIPLE GENETIC MECHANISMS FOR THE EVOLUTION OF SENESCENCE IN DROSOPHILA MELANOGASTER

We present the results of selection experiments designed to distinguish between antagonistic pleiotropy and mutation accumulation, two mechanisms for the evolution of senescence. Reverse selection for early-life fitness was applied to laboratory populations of Drosophila melanogaster that had been previously selected for late-life fitness. These populations also exhibited reduced early-age female fecundity and increased resistance to the stresses of starvation, desiccation, and ethanol, when compared to control populations. Reverse selection was carried out at both uncontrolled, higher larval rearing density and at controlled, lower larval density. In the uncontrolled-density selection lines, early-age female fecundity increased to control-population levels in response to the reintroduction of selection for early-age fitness. Concomitantly, resistance to starvation declined in agreement with previous observations of a negative genetic correlation between these two characters and in accordance with the antagonistic-pleiotropy mechanism. However, resistance to stresses of desiccation and ethanol did not decline in the uncontrolled-density lines during 22 generations of reverse selection for early-life fitness. The latter results provide evidence that mutation accumulation has also played a role in the evolution of senescence in this set of Drosophila populations. No significant response in early-age fecundity or starvation resistance was observed in the controlled-density reverse-selection lines, supporting previous observations that selection on Drosophila life-history characters is critically sensitive to larval rearing density.     

Gametic models for multitrait selection schemes to study variance of response and drift under adverse genetic correlations

A major issue faced by breeders is how to effectively manage adverse correlations in breeding programs. We present results of a Monte Carlo allele-based simulation of the changes in response and variance of response under adverse genetic correlations by using the examples of two contrasting selection methods: the ‘Smith-Hazel’ selection index (SH) and independent culling (IC). We assumed several gene models, which included linkage and antagonistic pleiotropy as the primary drivers of adverse genetic correlations. The different behaviors of these selection methods allowed us to identify the mechanism behind the generation of uncertainty under antagonistic trait selection: IC had the properties of stabilizing selection, while SH behaved more similar to disruptive selection. Although SH outperformed IC in terms of genetic gain, this advantage happened at the cost of higher variance of response and loss of heterozygosity. Using an optimum selection algorithm (OS) to prevent the loss of heterozygosity through a constraint on inbreeding in SH/OS increased marginally the reliability, remaining still below that of IC under equal conditions. However, SH/OS had lower inbreeding (ΔF) than IC for equivalent levels of genetic gain, so a compromise between high selection reliability, low ΔF, and gain must be made by a breeder under antagonistic trait selection even with the use of optimization tools.     

Multivariate intralocus sexual conflict in seed beetles

Intralocus sexual conflict (IaSC) is pervasive because males and females experience differences in selection but share much of the same genome. Traits with integrated genetic architecture should be reservoirs of sexually antagonistic genetic variation for fitness, but explorations of multivariate IaSC are scarce. Previously, we showed that upward artificial selection on male life span decreased male fitness but increased female fitness compared with downward selection in the seed beetle Callosobruchus maculatus. Here, we use these selection lines to investigate sex‐specific evolution of four functionally integrated traits (metabolic rate, locomotor activity, body mass, and life span) that collectively define a sexually dimorphic life‐history syndrome in many species. Male‐limited selection for short life span led to correlated evolution in females toward a more male‐like multivariate phenotype. Conversely, males selected for long life span became more female‐like, implying that IaSC results from genetic integration of this suite of traits. However, while life span, metabolism, and body mass showed correlated evolution in the sexes, activity did not evolve in males but, surprisingly, did so in females. This led to sexual monomorphism in locomotor activity in short‐life lines associated with detrimental effects in females. Our results thus support the general tenet that widespread pleiotropy generates IaSC despite sex‐specific genetic architecture.