Is local adaptation in Mimulus guttatus caused by trade‐offs at individual loci?

Local adaptation is considered to be the result of fitness trade‐offs for particular phenotypes across different habitats. However, it is unclear whether such phenotypic trade‐offs exist at the level of individual genetic loci. Local adaptation could arise from trade‐offs of alternative alleles at individual loci or by complementary sets of loci with different fitness effects of alleles in one habitat but selective neutrality in the alternative habitat. To evaluate the genome‐wide basis of local adaptation, we performed a field‐based quantitative trait locus (QTL) mapping experiment on recombinant inbred lines (RILs) created from coastal perennial and inland annual races of the yellow monkeyflower (Mimulus guttatus) grown reciprocally in native parental habitats. Overall, we detected 19 QTLs affecting one or more of 16 traits measured in two environments, most of small effect. We identified 15 additional QTL effects at two previously identified candidate QTLs [DIV ERGENCE (DIV)]. Significant QTL by environment interactions were detected at the DIV loci, which was largely attributable to genotypic differences at a single field site. We found no detectable evidence for trade‐offs for any one component of fitness, although DIV2 showed a trade‐off involving different fitness traits between sites, suggesting that local adaptation is largely controlled by non‐overlapping loci. This is surprising for an outcrosser, implying that reduced gene flow prevents the evolution of individuals adapted to multiple environments. We also determined that native genotypes were not uniformly adaptive, possibly reflecting fixed mutational load in one of the populations.     

STRONG SELECTION GENOME‐WIDE ENHANCES FITNESS TRADE‐OFFS ACROSS ENVIRONMENTS AND EPISODES OF SELECTION

Fitness trade‐offs across episodes of selection and environments influence life‐history evolution and adaptive population divergence. Documenting these trade‐offs remains challenging as selection can vary in magnitude and direction through time and space. Here, we evaluate fitness trade‐offs at the levels of the whole organism and the quantitative trait locus (QTL) in a multiyear field study of Boechera stricta (Brassicaceae), a genetically tractable mustard native to the Rocky Mountains. Reciprocal local adaptation was pronounced for viability, but not for reproductive components of fitness. Instead, local genomes had a fecundity advantage only in the high latitude garden. By estimating realized selection coefficients from individual‐level data on viability and reproductive success and permuting the data to infer significance, we examined the genetic basis of fitness trade‐offs. This analytical approach (Conditional Neutrality‐Antagonistic Pleiotropy, CNAP) identified genetic trade‐offs at a flowering phenology QTL (costs of adaptation) and revealed genetic trade‐offs across fitness components (costs of reproduction). These patterns would not have emerged from traditional ANOVA‐based QTL mapping. Our analytical framework can be applied to other systems to investigate fitness trade‐offs. This task is becoming increasingly important as climate change may alter fitness landscapes, potentially disrupting fitness trade‐offs that took many generations to evolve.     

QTL mapping of freezing tolerance: links to fitness and adaptive trade‐offs

Local adaptation, defined as higher fitness of local vs. nonlocal genotypes, is commonly identified in reciprocal transplant experiments. Reciprocally adapted populations display fitness trade‐offs across environments, but little is known about the traits and genes underlying fitness trade‐offs in reciprocally adapted populations. We investigated the genetic basis and adaptive significance of freezing tolerance using locally adapted populations of Arabidopsis thaliana from Italy and Sweden. Previous reciprocal transplant studies of these populations indicated that subfreezing temperature is a major selective agent in Sweden. We used quantitative trait locus (QTL) mapping to identify the contribution of freezing tolerance to previously demonstrated local adaptation and genetic trade‐offs. First, we compared the genomic locations of freezing tolerance QTL to those for previously published QTL for survival in Sweden, and overall fitness in the field. Then, we estimated the contributions to survival and fitness across both field sites of genotypes at locally adaptive freezing tolerance QTL. In growth chamber studies, we found seven QTL for freezing tolerance, and the Swedish genotype increased freezing tolerance for five of these QTL. Three of these colocalized with locally adaptive survival QTL in Sweden and with trade‐off QTL for overall fitness. Two freezing tolerance QTL contribute to genetic trade‐offs across environments for both survival and overall fitness. A major regulator of freezing tolerance, CBF2, is implicated as a candidate gene for one of the trade‐off freezing tolerance QTL. Our study provides some of the first evidence of a trait and gene that mediate a fitness trade‐off in nature.     

Adaptive divergence in flowering time among natural populations of Arabidopsis thaliana: Estimates of selection and QTL mapping

To identify the ecological and genetic mechanisms of local adaptation requires estimating selection on traits, identifying their genetic basis, and evaluating whether divergence in adaptive traits is due to conditional neutrality or genetic trade‐offs. To this end, we conducted field experiments for three years using recombinant inbred lines (RILs) derived from two ecotypes of Arabidopsis thaliana (Italy, Sweden), and at each parental site examined selection on flowering time and mapped quantitative trait loci (QTL). There was strong selection for early flowering in Italy, but weak selection in Sweden. Eleven distinct flowering time QTL were detected, and for each the Italian genotype caused earlier flowering. Twenty‐seven candidate genes were identified, two of which (FLC and VIN3) appear under major flowering time QTL in Italy. Seven of eight QTL in Italy with narrow credible intervals colocalized with previously reported fitness QTL, in comparison to three of four in Sweden. The results demonstrate that the magnitude of selection on flowering time differs strikingly between our study populations, that the genetic basis of flowering time variation is multigenic with some QTL of large effect, and suggest that divergence in flowering time between ecotypes is due mainly to conditional neutrality.     

Paths to selection on life history loci in different natural environments across the native range of Arabidopsis thaliana

Selection on quantitative trait loci (QTL) may vary among natural environments due to differences in the genetic architecture of traits, environment‐specific allelic effects or changes in the direction and magnitude of selection on specific traits. To dissect the environmental differences in selection on life history QTL across climatic regions, we grew a panel of interconnected recombinant inbred lines (RILs) of Arabidopsis thaliana in four field sites across its native European range. For each environment, we mapped QTL for growth, reproductive timing and development. Several QTL were pleiotropic across environments, three colocalizing with known functional polymorphisms in flowering time genes (CRY2, FRI and MAF2‐5), but major QTL differed across field sites, showing conditional neutrality. We used structural equation models to trace selection paths from QTL to lifetime fitness in each environment. Only three QTL directly affected fruit number, measuring fitness. Most QTL had an indirect effect on fitness through their effect on bolting time or leaf length. Influence of life history traits on fitness differed dramatically across sites, resulting in different patterns of selection on reproductive timing and underlying QTL. In two oceanic field sites with high prereproductive mortality, QTL alleles contributing to early reproduction resulted in greater fruit production, conferring selective advantage, whereas alleles contributing to later reproduction resulted in larger size and higher fitness in a continental site. This demonstrates how environmental variation leads to change in both QTL effect sizes and direction of selection on traits, justifying the persistence of allelic polymorphism at life history QTL across the species range.     

Evolution of Drosophila resistance against different pathogens and infection routes entails no detectable maintenance costs

Pathogens exert a strong selective pressure on hosts, entailing host adaptation to infection. This adaptation often affects negatively other fitness‐related traits. Such trade‐offs may underlie the maintenance of genetic diversity for pathogen resistance. Trade‐offs can be tested with experimental evolution of host populations adapting to parasites, using two approaches: (1) measuring changes in immunocompetence in relaxed‐selection lines and (2) comparing life‐history traits of evolved and control lines in pathogen‐free environments. Here, we used both approaches to examine trade‐offs in Drosophila melanogaster populations evolving for over 30 generations under infection with Drosophila C Virus or the bacterium Pseudomonas entomophila, the latter through different routes. We find that resistance is maintained after up to 30 generations of relaxed selection. Moreover, no differences in several classical life‐history traits between control and evolved populations were found in pathogen‐free environments, even under stresses such as desiccation, nutrient limitation, and high densities. Hence, we did not detect any maintenance costs associated with resistance to pathogens. We hypothesize that extremely high selection pressures commonly used lead to the disproportionate expression of costs relative to their actual occurrence in natural systems. Still, the maintenance of genetic variation for pathogen resistance calls for an explanation.     

The extent and genetic basis of phenotypic divergence in life history traits in Mimulus guttatus

Differential natural selection acting on populations in contrasting environments often results in adaptive divergence in multivariate phenotypes. Multivariate trait divergence across populations could be caused by selection on pleiotropic alleles or through many independent loci with trait‐specific effects. Here, we assess patterns of association between a suite of traits contributing to life history divergence in the common monkey flower, Mimulus guttatus, and examine the genetic architecture underlying these correlations. A common garden survey of 74 populations representing annual and perennial strategies from across the native range revealed strong correlations between vegetative and reproductive traits. To determine whether these multitrait patterns arise from pleiotropic or independent loci, we mapped QTLs using an approach combining high‐throughput sequencing with bulk segregant analysis on a cross between populations with divergent life histories. We find extensive pleiotropy for QTLs related to flowering time and stolon production, a key feature of the perennial strategy. Candidate genes related to axillary meristem development colocalize with the QTLs in a manner consistent with either pleiotropic or independent QTL effects. Further, these results are analogous to previous work showing pleiotropy‐mediated genetic correlations within a single population of M. guttatus experiencing heterogeneous selection. Our findings of strong multivariate trait associations and pleiotropic QTLs suggest that patterns of genetic variation may determine the trajectory of adaptive divergence.     

THE GENOMIC ARCHITECTURE OF SEXUAL DIMORPHISM IN THE DIOECIOUS PLANT SILENE LATIFOLIA

Evaluating the genetic architecture of sexual dimorphism can aid our understanding of the extent to which shared genetic control of trait variation versus sex‐specific control impacts the evolutionary dynamics of phenotypic change within each sex. We performed a QTL analysis on Silene latifolia to evaluate the contribution of sex‐specific QTL to phenotypic variation in 46 traits, whether traits involved in trade‐offs had colocalized QTL, and whether the distribution of sex‐specific loci can explain differences between the sexes in their variance/covariance matrices. We used a backcross generation derived from two artificial‐selection lines. We found that sex‐specific QTL explained a significantly greater percent of the variation in sexually dimorphic traits than loci expressed in both sexes. Genetically correlated traits often had colocalized QTL, whose signs were in the expected direction. Lastly, traits with different genetic correlations within the sexes displayed a disproportionately high number of sex‐specific QTL, and more QTL co‐occurred in males than females, suggesting greater trait integration. These results show that sex differences in QTL patterns are congruent with theory on the resolution of sexual conflict and differences based on G ‐matrix results. They also suggest that trade‐offs and trait integration are likely to affect males more than females.     

Effects of variation in resource acquisition during different stages of the life cycle on life‐history traits and trade‐offs in a burying beetle

Individual variation in resource acquisition should have consequences for life‐history traits and trade‐offs between them because such variation determines how many resources can be allocated to different life‐history functions, such as growth, survival and reproduction. Since resource acquisition can vary across an individual's life cycle, the consequences for life‐history traits and trade‐offs may depend on when during the life cycle resources are limited. We tested for differential and/or interactive effects of variation in resource acquisition in the burying beetle Nicrophorus vespilloides. We designed an experiment in which individuals acquired high or low amounts of resources across three stages of the life cycle: larval development, prior to breeding and the onset of breeding in a fully crossed design. Resource acquisition during larval development and prior to breeding affected egg size and offspring survival, respectively. Meanwhile, resource acquisition at the onset of breeding affected size and number of both eggs and offspring. In addition, there were interactive effects between resource acquisition at different stages on egg size and offspring survival. However, only when females acquired few resources at the onset of breeding was there evidence for a trade‐off between offspring size and number. Our results demonstrate that individual variation in resource acquisition during different stages of the life cycle has important consequences for life‐history traits but limited effects on trade‐offs. This suggests that in species that acquire a fixed‐sized resource at the onset of breeding, the size of this resource has larger effects on life‐history trade‐offs than resources acquired at earlier stages.     

Repeated evolution of local adaptation in swimming performance: population‐level trade‐offs between burst and endurance swimming in Brachyrhaphis freshwater fish

Specialization is fundamentally important in biology because specialized traits allow species to expand into new environments, in turn promoting population differentiation and speciation. Specialization often results in trade‐offs between traits that maximize fitness in one environment but not others. Despite the ubiquity of trade‐offs, we know relatively little about how consistently trade‐offs evolve between populations when multiple sets of populations experience similarly divergent selective regimes. In the present study, we report a case study on Brachyrhaphis fishes from different predation environments. We evaluate apparent within/between population trade‐offs in burst‐speed and endurance at two levels of evolutionary diversification: high‐ and low‐predation populations of Brachyrhaphis rhabdophora, and sister species Brachyrhaphis roseni and Brachyrhaphis terrabensis, which occur in high‐ and low‐predation environments, respectively. Populations of Brachyrhaphis experiencing different predation regimes consistently evolved swimming specializations indicative of a trade‐off between two swimming forms that are likely highly adaptive in the environment in which they occur. We show that populations have become similarly locally adapted at both levels of diversification, suggesting that swimming specialization has evolved rather rapidly and persisted post‐speciation. Our findings provide valuable insight into how local adaptation evolves at different stages of evolutionary divergence.     

Fitness costs of herbicide resistance across natural populations of the common morning glory,Ipomoea purpurea

Although fitness costs associated with plant defensive traits are widely expected, they are not universally detected, calling into question their generality. Here, we examine the potential for life‐history trade‐offs associated with herbicide resistance by examining seed germination, root growth, and above‐ground growth across 43 naturally occurring populations of Ipomoea purpurea that vary in their resistance to RoundUp ® , the most commonly used herbicide worldwide. We find evidence for life‐history trade‐offs associated with all three traits; highly resistant populations had lower germination, shorter roots, and smaller above‐ground size. A visual exploration of the data indicated that the type of trade‐off may differ among populations. Our results demonstrate that costs of adaptation may be present at stages other than simply the production of progeny in this agricultural weed. Additionally, the cumulative effect of costs at multiple life cycle stages can result in severe consequences to fitness when adapting to novel environments.     

Assortative mating by flowering time and its effect on correlated traits in variable environments

Reproductive timing is a key life‐history trait that impacts the pool of available mates, the environment experienced during flowering, and the expression of other traits through genetic covariation. Selection on phenology, and its consequences on other life‐history traits, has considerable implications in the context of ongoing climate change and shifting growing seasons. To test this, we grew field‐collected seed from the wildflower Mimulus guttatus in a greenhouse to assess the standing genetic variation for flowering time and covariation with other traits. We then created full‐sib families through phenological assortative mating and grew offspring in three photoperiod treatments representing seasonal variation in daylength. We find substantial quantitative genetic variation for the onset of flowering time, which covaried with vegetative traits. The assortatively‐mated offspring varied in their critical photoperiod by over two hours, so that families differed in their probability of flowering across treatments Allocation to flowering and vegetative growth changed across the daylength treatments, with consistent direction and magnitude of covariation among flowering time and other traits. Our results suggest that future studies of flowering time evolution should consider the joint evolution of correlated traits and shifting seasonal selection to understand how environmental variation influences life histories.     

Connecting thermal performance curve variation to the genotype: a multivariate QTL approach

Thermal performance curves (TPCs) are continuous reaction norms that describe the relationship between organismal performance and temperature and are useful for understanding trade‐offs involved in thermal adaptation. Although thermal trade‐offs such as those between generalists and specialists or between hot‐ and cold‐adapted phenotypes are known to be genetically variable and evolve during thermal adaptation, little is known of the genetic basis to TPCs – specifically, the loci involved and the directionality of their effects across different temperatures. To address this, we took a multivariate approach, mapping quantitative trait loci (QTL) for locomotor activity TPCs in the fly, Drosophila serrata, using a panel of 76 recombinant inbred lines. The distribution of additive genetic (co)variance in the mapping population was remarkably similar to the distribution of mutational (co)variance for these traits. We detected 11 TPC QTL in females and 4 in males. Multivariate QTL effects were closely aligned with the major axes genetic (co)variation between temperatures; most QTL effects corresponded to variation for either overall increases or decreases in activity with a smaller number indicating possible trade‐offs between activity at high and low temperatures. QTL representing changes in curve shape such as the ‘generalist–specialist’ trade‐off, thought key to thermal adaptation, were poorly represented in the data. We discuss these results in the light of genetic constraints on thermal adaptation.     

Environmental effects on the covariation among pace‐of‐life traits

Pace‐of‐life syndromes (POLSs) are suites of life‐history, physiological and behavioural traits that arise due to trade‐offs between allocation to current and future reproduction. Traits generally show covariation that can arise from genetic and environmental influences on phenotypes and constrain the independent evolution of traits, resulting in fitness consequences and impacts on population dynamics. The notion that correlations among traits may vary among populations along environmental gradients suggests an important role for the environment in shaping and maintaining POLSs. However, no synthesis has been attempted of the myriad ways in which environmental factors should influence POLSs. Here, we formulate a series of hypotheses targeting the critical interfaces of the environment and life‐history ‐ behaviour associations across different organisms. We discuss the hypotheses in light of findings from a systematic review of studies that measured changes in the association between behaviour and life‐history traits as a function of environmental conditions. The review revealed that POLSs are often shaped by environmental variation, where harshness of the environment in early life has the most consistent effects on POLS. However, only partial or no effects of environmental variation were found in a number of studies, which may result from the highly variable study systems, traits and environments studied. We highlight promising directions arising from the available studies and identify knowledge gaps that, if unaddressed, will impede progress in the field.     

Localization of quantitative trait loci for diapause and other photoperiodically regulated life history traits important in adaptation to seasonally varying environments

Seasonally changing environments at high latitudes present great challenges for the reproduction and survival of insects, and photoperiodic cues play an important role in helping them to synchronize their life cycle with prevalent and forthcoming conditions. We have mapped quantitative trait loci (QTL) responsible for the photoperiodic regulation of four life history traits, female reproductive diapause, cold tolerance, egg‐to‐eclosion development time and juvenile body weight in Drosophila montana strains from different latitudes in Canada and Finland. The F2 progeny of the cross was reared under a single photoperiod (LD cycle 16:8), which the flies from the Canadian population interpret as early summer and the flies from the Finnish population as late summer. The analysis revealed a unique QTL for diapause induction on the X chromosome and several QTL for this and the other measured traits on the 4th chromosome. Flies’ cold tolerance, egg‐to‐eclosion development time and juvenile body weight had several QTL also on the 2nd, 3rd and 5th chromosome, some of the peaks overlapping with each other. These results suggest that while the downstream output of females’ photoperiodic diapause response is partly under a different genetic control from that of the other traits in the given day length, all traits also share some QTL, possibly involving genes with pleiotropic effects and/or multiple tightly linked genes. Nonoverlapping QTL detected for some of the traits also suggest that the traits are potentially capable of independent evolution, even though this may be restricted by epistatic interactions and/or correlations and trade‐offs between the traits.     

Stressful environments can indirectly select for increased longevity

Longevity is modulated by a range of conserved genes in eukaryotes, but it is unclear how variation in these genes contributes to the evolution of longevity in nature. Mutations that increase life span in model organisms typically induce trade‐offs which lead to a net reduction in fitness, suggesting that such mutations are unlikely to become established in natural populations. However, the fitness consequences of manipulating longevity have rarely been assessed in heterogeneous environments, in which stressful conditions are encountered. Using laboratory selection experiments, we demonstrate that long‐lived, stress‐resistant Caenorhabditis elegans age‐1(hx546) mutants have higher fitness than the wild‐type genotype if mixed genotype populations are periodically exposed to high temperatures when food is not limited. We further establish, using stochastic population projection models, that the age‐1(hx546) mutant allele can confer a selective advantage if temperature stress is encountered when food availability also varies over time. Our results indicate that heterogeneity in environmental stress may lead to altered allele frequencies over ecological timescales and indirectly drive the evolution of longevity. This has important implications for understanding the evolution of life‐history strategies.     

Partitioning of resources: the evolutionary genetics of sexual conflict over resource acquisition and allocation

Fitness depends on both the resources that individuals acquire and the allocation of those resources to traits that influence survival and reproduction. Optimal resource allocation differs between females and males as a consequence of their fundamentally different reproductive strategies. However, because most traits have a common genetic basis between the sexes, conflicting selection between the sexes over resource allocation can constrain the evolution of optimal allocation within each sex, and generate trade‐offs for fitness between them (i.e. ‘sexual antagonism’ or ‘intralocus sexual conflict’). The theory of resource acquisition and allocation provides an influential framework for linking genetic variation in acquisition and allocation to empirical evidence of trade‐offs between distinct life‐history traits. However, these models have not considered the emergence of trade‐offs within the context of sexual dimorphism, where they are expected to be particularly common. Here, we extend acquisition–allocation theory and develop a quantitative genetic framework for predicting genetically based trade‐offs between life‐history traits within sexes and between female and male fitness. Our models demonstrate that empirically measurable evidence of sexually antagonistic fitness variation should depend upon three interacting factors that may vary between populations: (1) the genetic variances and between‐sex covariances for resource acquisition and allocation traits, (2) condition‐dependent expression of resource allocation traits and (3) sex differences in selection on the allocation of resource to different fitness components.     

Genetic variation in flowering phenology and avoidance of seed predation in native populations of Ulex europaeus

The genetic variation in flowering phenology may be an important component of a species’ capacity to colonize new environments. In native populations of the invasive species Ulex europaeus, flowering phenology has been shown to be bimodal and related to seed predation. The aim of the present study was to determine if this bimodality has a genetic basis, and to investigate whether the polymorphism in flowering phenology is genetically linked to seed predation, pod production and growth patterns. We set up an experiment raising maternal families in a common garden. Based on mixed analyses of variance and correlations among maternal family means, we found genetic differences between the two main flowering types and confirmed that they reduced seed predation in two different ways: escape in time or predator satiation. We suggest that this polymorphism in strategy may facilitate maintain high genetic diversity for flowering phenology and related life‐history traits in native populations of this species, hence providing high evolutionary potential for these traits in invaded areas.     

Fitness effects of mutation: testing genetic redundancy in Arabidopsis thaliana

Screens of organisms with disruptive mutations in a single gene often fail to detect phenotypic consequences for the majority of mutants. One explanation for this phenomenon is that the presence of paralogous loci provides genetic redundancy. However, it is also possible that the assayed traits are affected by few loci, that effects could be subtle or that phenotypic effects are restricted to certain environments. We assayed a set of T‐DNA insertion mutant lines of Arabidopsis thaliana to determine the frequency with which mutation affected fitness‐related phenotypes. We found that between 8% and 42% of the assayed lines had altered fitness from the wild type. Furthermore, many of these lines exhibited fitness greater than the wild type. In a second experiment, we grew a subset of the lines in multiple environments and found whether a T‐DNA insert increased or decreased fitness traits depended on the assay environment. Overall, our evidence contradicts the hypothesis that genetic redundancy is a common phenomenon in A. thaliana for fitness traits. Evidence for redundancy from prior screens of knockout mutants may often be an artefact of the design of the phenotypic assays which have focused on less complex phenotypes than fitness and have used single environments. Finally, our study adds to evidence that beneficial mutations may represent a significant component of the mutational spectrum of A. thaliana.     

Life‐history trade‐offs vary with resource availability across the geographic range of a widespread plant

• Trade‐offs between reproduction, growth and survival arise from limited resource availability in plants. Environmental stress is expected to exacerbate these negative correlations, but no studies have evaluated variation in life‐history trade‐offs throughout species geographic ranges. Here we analyse the costs of growth and reproduction across the latitudinal range of the widespread herb Plantago coronopus in Europe.
• We monitored the performance of thousands of individuals in 11 populations of P. coronopus, and tested whether the effects of growth and reproduction on a set of vital rates (growth, probability of survival, probability of reproduction and fecundity) varied with local precipitation and soil fertility. To account for variation in internal resources among individuals, we analysed trade‐offs correcting for differences in size.
• Growth was negatively affected by previous growth and reproduction. We also found costs of growth and reproduction on survival, reproduction probability and fecundity, but only in populations with low soil fertility. Costs also increased with precipitation, possibly due to flooding‐related stress. In contrast, growth was positively correlated with subsequent survival, and there was a positive covariation in reproduction between consecutive years under certain environments, a potential strategy to exploit temporary benign conditions.
• Overall, we found both negative and positive correlations among vital rates across P. coronopus geographic range. Trade‐offs predominated under stressful conditions, and positive correlations arose particularly between related traits like reproduction investment across years. By analysing multiple and diverse fitness components along stress gradients, we can better understand life‐history evolution across species’ ranges, and their responses to environmental change.