Genetic analysis of life-history constraint and evolution in a wild ungulate population

Trade-offs among life-history traits are central to evolutionary theory. In quantitative genetic terms, trade-offs may be manifested as negative genetic covariances relative to the direction of selection on phenotypic traits. Although the expression and selection of ecologically important phenotypic variation are fundamentally multivariate phenomena, the in situ quantification of genetic covariances is challenging. Even for life-history traits, where well-developed theory exists with which to relate phenotypic variation to fitness variation, little evidence exists from in situ studies that negative genetic covariances are an important aspect of the genetic architecture of life-history traits. In fact, the majority of reported estimates of genetic covariances among life-history traits are positive. Here we apply theory of the genetics and selection of life histories in organisms with complex life cycles to provide a framework for quantifying the contribution of multivariate genetically based relationships among traits to evolutionary constraint. We use a Bayesian framework to link pedigree-based inference of the genetic basis of variation in life-history traits to evolutionary demography theory regarding how life histories are selected. Our results suggest that genetic covariances may be acting to constrain the evolution of female life-history traits in a wild population of red deer Cervus elaphus: genetic covariances are estimated to reduce the rate of adaptation by about 40%, relative to predicted evolutionary change in the absence of genetic covariances. Furthermore, multivariate phenotypic (rather than genetic) relationships among female life-history traits do not reveal this constraint.     

Conflicting processes in the evolution of body size and development time

Body size and development time of Manduca sexta are both determined by the same set of three developmental–physiological factors. These define a parameter space within which it is possible to analyse and explain how phenotypic change is associated with changes in the underlying factors. Body size and development time are determined by the identical set of underlying factors, so they are not independent, but because the mechanisms by which these factors produce each phenotype are different, the two phenotypes are only weakly correlated, and the correlation is context dependent. We use a mathematical model of this mechanism to explore the association between body size and development time and show that the correlation between these two life-history traits can be positive, zero or negative, depending entirely on where in parameter space a population is located, and on which of the underlying factors has a greater variation. The gradient within this parameter space predicts the unconstrained evolutionary trajectory under directional selection on each trait. Calculations of the gradients for body size and development time revealed that these are nearly orthogonal through much of the parameter space. Therefore, simultaneous directional selection on body size and development time can be neither synergistic nor antagonistic but leads to conflicting selection on the underlying developmental parameters.     

Evolution of pleiotropic alleles for maturation and size as a consequence of predation

Understanding life-history evolution requires knowledge about genetic interactions, physiological mechanisms and the nature of selection. For platyfish, Xiphophorus maculatus, extensive information is available about genetic and physiological mechanisms influencing life-history traits. In particular, alleles at the pituitary locus have large and antagonistic effects on age and size at sexual maturation. To examine how predation affects the evolution of these antagonistic traits, I examined pituitary allele evolution in experimental populations differing in predation risk. A smaller size, earlier maturation allele increased in frequency when predators were absent, while a larger size, later maturation allele increased in frequency when predators were present. Thus, predation favours alleles for larger size, at the cost of later maturation and reproduction. These findings are interesting for several reasons. First, predation is often predicted to favour early reproduction at smaller sizes. Second, few studies have shown how selection acts on alleles that affect age and size at sexual maturation. Finally, many studies assume that trade-offs between these life-history traits result from antagonistic pleiotropy, with alleles that positively affect one trait negatively affecting another, yet this is rarely known. This study unequivocally demonstrates that genetically based trade-offs affect life-history evolution in platyfish.     

WATER STRESS ALTERS THE GENETIC ARCHITECTURE OF FUNCTIONAL TRAITS ASSOCIATED WITH DROUGHT ADAPTATION IN AVENA BARBATA

Environmental stress can alter genetic variation and covariation underlying functional traits, and thus affect adaptive evolution in response to natural selection. However, the genetic basis of functional traits is rarely examined in contrasting resource environments, and consequently, there is no consensus regarding whether environmental stress constrains or facilitates adaptive evolution. We tested whether resource availability affects genetic variation for and covariation among seven physiological traits and seven morphological/performance traits by growing the annual grass Avena barbata in dry and well-watered treatments. We found that differences in the overall genetic variance–covariance ( G ) matrix between environments were driven by physiological traits rather than morphology and performance traits. More physiological traits were heritable in the dry treatment than the well-watered treatment and many of the genetic correlations among physiological traits were environment dependent. In contrast, genetic variation and covariation among the morphological and performance traits did not differ across treatments. Furthermore, genetic correlations between physiology and performance were stronger in the dry treatment, which contributed to differences in the overall G -matrix. Our results therefore suggest that physiological adaptation would be constrained by low heritable variation in resource-rich environments, but facilitated by higher heritable variation and stronger genetic correlations with performance traits in resource-poor environments.     

Personality and the emergence of the pace-of-life syndrome concept at the population level

The pace-of-life syndrome (POLS) hypothesis specifies that closely related species or populations experiencing different ecological conditions should differ in a suite of metabolic, hormonal and immunity traits that have coevolved with the life-history particularities related to these conditions. Surprisingly, two important dimensions of the POLS concept have been neglected: (i) despite increasing evidence for numerous connections between behavioural, physiological and life-history traits, behaviours have rarely been considered in the POLS yet; (ii) the POLS could easily be applied to the study of covariation among traits between individuals within a population. In this paper, we propose that consistent behavioural differences among individuals, or personality, covary with life history and physiological differences at the within-population, interpopulation and interspecific levels. We discuss how the POLS provides a heuristic framework in which personality studies can be integrated to address how variation in personality traits is maintained within populations.     

GENETIC VARIATION FOR PHENOTYPIC PLASTICITY IN THE LARVAL LIFE HISTORY OF SPADEFOOT TOADS (SCAPHIOPUS COUCHII)

Phenotypic plasticity in life-history traits is common. The relationship between phenotype and environment, or reaction norm, associated with life-history plasticity can evolve by natural selection if there is genetic variation within a population for the reaction norm and if the traits involved affect fitness. As with other traits, selection on plasticity in a particular trait or in response to a particular environmental factor may be constrained by trade-offs with other traits that affect fitness. In this paper, I experimentally evaluated broad-sense genetic variation in the reaction norms of age and size at metamorphosis in response to two environmental factors, food level and temperature. Differences among full-sib families in one or both traits were evident in all treatments. However, variation among families in their responses to each treatment (genotype-environment interaction) resulted in variation among treatments in estimated heritabilities and genetic correlations. Age at metamorphosis was equally sensitive to temperature in all families, but size at metamorphosis was more sensitive to temperature in some families than in others. Size at metamorphosis was equally sensitive to food level in all families, but age at metamorphosis was sensitive to food in some families but not in others. At high temperature or low food, the genetic correlation between age and size at metamorphosis was positive, generating a potential trade-off between metamorphosing early to attain higher larval survival and metamorphosing later to achieve larger size. This trade-off extends across treatments: families with the largest average size at metamorphosis achieved larger size with the longest average and greatest plasticity in age at metamorphosis. Other families achieved shorter average larval periods by exhibiting greater plasticity in size at metamorphosis but had the smallest average size at metamorphosis. This trade-off may reflect an underlying functional constraint on the ability to respond optimally to all environments, resulting in persistent genetic variation in reaction norms.     

Effects of spontaneous mutation accumulation on sex ratio traits in a parasitoid wasp

Sex allocation theory has proved extremely successful at predicting when individuals should adjust the sex of their offspring in response to environmental conditions. However, we know rather little about the underlying genetics of sex ratio or how genetic architecture might constrain adaptive sex-ratio behavior. We examined how mutation influenced genetic variation in the sex ratios produced by the parasitoid wasp Nasonia vitripennis. In a mutation accumulation experiment, we determined the mutability of sex ratio, and compared this with the amount of genetic variation observed in natural populations. We found that the mutability (h(2)(m)) ranges from 0.001 to 0.002, similar to estimates for life-history traits in other organisms. These estimates suggest one mutation every 5-60 generations, which shift the sex ratio by approximately 0.01 (proportion males). In this and other studies, the genetic variation in N. vitripennis sex ratio ranged from 0.02 to 0.17 (broad-sense heritability, H(2)). If sex ratio is maintained by mutation-selection balance, a higher genetic variance would be expected given our mutational parameters. Instead, the observed genetic variance perhaps suggests additional selection against sex-ratio mutations with deleterious effects on other fitness traits as well as sex ratio (i.e., pleiotropy), as has been argued to be the case more generally.     

Genetic architecture of a selection response in Arabidopsis thaliana

Quantitative trait locus (QTL) mapping has become an established and effective method for studying the genetic architecture of complex traits. In this report, we use a QTL mapping approach in combination with data from a large selection experiment in Arabidopsis thaliana to explore a response to selection of experimental populations with differentiated genetic backgrounds. Experimental populations with genetic backgrounds derived from ecotypes Landsberg and Niederzenz were exposed to multiple generations of fertility and viability selection. This selection resulted in phenotypic shifts in a number of life-history and fitness-related characters including early development time, flowering time, dry biomass, longevity, and fruit production. Quantitative trait loci were mapped for these traits and their positions were compared to previously characterized allele frequency changes in the experimental populations (Ungerer et al. 2003). Quantitative trait locus positions largely colocalized with genomic regions under strong and consistent selection in populations with differentiated genetic backgrounds, suggesting that alleles for these traits were selected similarly in differentiated genetic backgrounds. However, one QTL region exhibited a more variable response; being positively selected on one genetic background but apparently neutral in another. This study demonstrates how QTL mapping approaches can be combined with map-based population genetic data to study how selection acts on standing genetic variation in populations.     

Niche construction through germination cueing: life-history responses to timing of germination in Arabidopsis thaliana

Germination responses to seasonal conditions determine the environment experienced by postgermination life stages, and this ability has potential consequences for the evolution of plant life histories. Using recombinant inbred lines of Arabidopsis thaliana, we tested whether life-history characters exhibited plasticity to germination timing, whether germination timing influenced the strength and mode of natural selection on life-history traits, and whether germination timing influenced the expression of genetic variation for life-history traits. Adult life-history traits exhibited strong plasticity to season of germination, and season of germination significantly altered the strength, mode, and even direction of selection on life-history traits under some conditions. None of the average plastic responses to season of germination or season of dispersal were adaptive, although some genotypes within our sample did exhibit adaptive responses. Thus, recombination between inbred lineages created some novel adaptive genotypes with improved responses to the seasonal timing of germination under some, but not all, conditions. Genetically based variation in germination time tended to augment genetic variances of adult life-history traits, but it did not increase the heritabilities because it also increased environmentally induced variance. Under some conditions, plasticity of life-history traits in response to genetically variable germination timing actually obscured genetic variation for those traits. Therefore, the evolution of germination responses can influence the evolution of life histories in a general manner by altering natural selection on life-history traits and the genetic variation of these traits.     

Resolving the genetic basis of invasiveness and predicting invasions

Considerable effort has been invested in determining traits underlying invasiveness. Yet, identifying a set of traits that commonly confers invasiveness in a range of species has proven elusive, and almost nothing is known about genetic loci affecting invasive success. Incorporating genetic model organisms into ecologically relevant studies is one promising avenue to begin dissecting the genetic underpinnings of invasiveness. Molecular biologists are rapidly characterizing genes mediating developmental responses to diverse environmental cues, i.e., genes for plasticity, as well as to environmental factors likely to impose strong selection on invading species, e.g., resistance to herbivores and competitors, coordination of life-history events with seasonal changes, and physiological tolerance of heat, drought, or cold. Here, we give an overview of molecular genetic tools increasingly used to characterize the genetic basis of adaptation and that may be used to begin identifying genetic mechanisms of invasiveness. Given the divergent traits that affect invasiveness, “invasiveness genes” common to many clades are unlikely, but the combination of developmental genetic advances with further evolutionary studies and modeling may provide a framework for identifying genes that account for invasiveness in related species.     

Genetic and physiological bases for phenological responses to current and predicted climates

We are now reaching the stage at which specific genetic factors with known physiological effects can be tied directly and quantitatively to variation in phenology. With such a mechanistic understanding, scientists can better predict phenological responses to novel seasonal climates. Using the widespread model species Arabidopsis thaliana, we explore how variation in different genetic pathways can be linked to phenology and life-history variation across geographical regions and seasons. We show that the expression of phenological traits including flowering depends critically on the growth season, and we outline an integrated life-history approach to phenology in which the timing of later life-history events can be contingent on the environmental cues regulating earlier life stages. As flowering time in many plants is determined by the integration of multiple environmentally sensitive gene pathways, the novel combinations of important seasonal cues in projected future climates will alter how phenology responds to variation in the flowering time gene network with important consequences for plant life history. We discuss how phenology models in other systems—both natural and agricultural—could employ a similar framework to explore the potential contribution of genetic variation to the physiological integration of cues determining phenology.     

Constraints on the evolution of function‐valued traits: a study of growth in Tribolium castaneum

Growth trajectories often impact individual fitness. They are continuous by nature and so are amenable to analysis using a function‐valued (FV) trait framework to reveal their underlying genetic architecture. Previous studies have found high levels of standing additive genetic (co)variance for growth trajectories despite the expectation that growth should be responding to frequent strong directional selection. In this study, the FV framework is used to estimate the additive genetic covariance function for growth trajectories in larval Tribolium castaneum to address questions about standing additive genetic (co)variance and possible evolutionary constraints on growth and to predict responses to four plausible selection regimes. Results show that additive genetic (co)variance is high at the early ages, but decreases towards later ages in the larval period. A selection gradient function of the same size and in the same direction of the first eigenfunction of the G‐function should give the maximal response. However, evolutionary constraints may be acting to keep this maximal response from being realized, through either conflicting effects on survivability and fecundity of larger body size, few evolutionary directions having sufficient additive variance for a response, genetic trade‐offs with other traits or physiological regulatory mechanisms. More light may be shed on these constraints through the development of more sophisticated statistical approaches and implementation of additional empirical studies to explicitly test for specific types of constraints.     

The genetic basis of smoltification-related traits in Oncorhynchus mykiss

The timing and propensity for migration between fresh- and seawater is a key theme in the diversity of life histories within the salmonid fishes. Across salmonid species, life-history strategies range from wholly freshwater-resident populations, to migratory and nonmigratory variation within populations, to populations and species that are primarily migratory. Despite the central theme of migration to the evolution of these fishes, the genetic architecture of migration-related processes is poorly understood. Using a genetic cross of clonal lines derived from migratory and nonmigratory life-history types of Onchorhynchus mykiss (steelhead and rainbow trout, respectively), we have dissected the genetic architecture of the complex physiological and morphological transformation that occurs immediately prior to seaward migration (termed smoltification). Quantitative trait loci (QTL) analyses were used to identify the number, effects, and genomic location of loci associated with smoltification-related traits, including growth and condition factor, body coloration, morphology, and osmoregulatory enzymes during the smoltification period. Genetic analyses revealed numerous QTL, but one locus in particular is associated with multiple traits in single and joint analyses. Dissecting the genetic architecture of this highly complex trait has profound implications for understanding the genetic and evolutionary basis of life-history diversity within and among migratory fishes.     

Correlated evolution of life-history with size at maturity in Daphnia pulicaria: patterns within and between populations

Explaining the repeated evolution of similar sets of traits under similar environmental conditions is an important issue in evolutionary biology. The extreme alternative classes of explanations for correlated suites of traits are optimal adaptation and genetic constraint resulting from pleiotropy. Adaptive explanations presume that individual traits are free to evolve to their local optima and that convergent evolution represents particularly adaptive combinations of traits. Alternatively, if pleiotropy is strong and difficult to break, strong selection on one or a few particularly important characters would be expected to result in consistent correlated evolution of associated traits. If pleiotropy is common, we predict that the pattern of divergence among populations will consistently reflect the within-population genetic architecture. To test the idea that the multivariate life-history phenotype is largely a byproduct of strong selection on body size, we imposed divergent artificial selection on size at maturity upon two populations of the cladoceran Daphnia pulicaria, chosen on the basis of their extreme divergence in body size. Overall, the trajectory of divergence between the two natural populations did not differ from that predicted by the genetic architecture within each population. However, the pattern of correlated responses suggested the presence of strong pleiotropic constraints only for adult body size and not for other life-history traits. One trait, offspring size, appears to have evolved in a way different from that expected from the within-population genetic architecture and may be under stabilizing selection.     

The alignment between phenotypic plasticity,the major axis of genetic variation and the response to selection

Phenotypic plasticity is the ability of a genotype to produce more than one phenotype in order to match the environment. Recent theory proposes that the major axis of genetic variation in a phenotypically plastic population can align with the direction of selection. Therefore, theory predicts that plasticity directly aids adaptation by increasing genetic variation in the direction favoured by selection and reflected in plasticity. We evaluated this theory in the freshwater crustacean Daphnia pulex, facing predation risk from two contrasting size-selective predators. We estimated plasticity in several life-history traits, the G matrix of these traits, the selection gradients on reproduction and survival, and the predicted responses to selection. Using these data, we tested whether the genetic lines of least resistance and the predicted response to selection aligned with plasticity. We found predator environment-specific G matrices, but shared genetic architecture across environments resulted in more constraint in the G matrix than in the plasticity of the traits, sometimes preventing alignment of the two. However, as the importance of survival selection increased, the difference between environments in their predicted response to selection increased and resulted in closer alignment between the plasticity and the predicted selection response. Therefore, plasticity may indeed aid adaptation to new environments.     

Optimal annual routines: behaviour in the context of physiology and ecology

Organisms in a seasonal environment often schedule activities in a regular way over the year. If we assume that such annual routines have been shaped by natural selection then life-history theory should provide a basis for explaining them. We argue that many life-history trade-offs are mediated by underlying physiological variables that act on various time scales. The dynamics of these variables often preclude considering one period of the year in isolation. In order to capture the essence of annual routines, and many life-history traits, a detailed model of changes in physiological state over the annual cycle is required. We outline a modelling approach based on suitable physiological and ecological state variables that can capture this underlying biology, and describe how models based on this approach can be used to generate a range of insights and predictions.     

The genetic covariance among clinal environments after adaptation to an environmental gradient in Drosophila serrata

We examined the genetic basis of clinal adaptation by determining the evolutionary response of life-history traits to laboratory natural selection along a gradient of thermal stress in Drosophila serrata. A gradient of heat stress was created by exposing larvae to a heat stress of 36 degrees for 4 hr for 0, 1, 2, 3, 4, or 5 days of larval development, with the remainder of development taking place at 25 degrees. Replicated lines were exposed to each level of this stress every second generation for 30 generations. At the end of selection, we conducted a complete reciprocal transfer experiment where all populations were raised in all environments, to estimate the realized additive genetic covariance matrix among clinal environments in three life-history traits. Visualization of the genetic covariance functions of the life-history traits revealed that the genetic correlation between environments generally declined as environments became more different and even became negative between the most different environments in some cases. One exception to this general pattern was a life-history trait representing the classic trade-off between development time and body size, which responded to selection in a similar genetic fashion across all environments. Adaptation to clinal environments may involve a number of distinct genetic effects along the length of the cline, the complexity of which may not be fully revealed by focusing primarily on populations at the ends of the cline.     

A behavioral perspective on fishing-induced evolution

The potential for excessive and/or selective fishing to act as an evolutionary force has been emphasized recently. However, most studies have focused on evolution of life-history traits in response to size-selective harvesting. Here we draw attention to fishing-induced evolution of behavioral and underlying physiological traits. We contend that fishing-induced selection directly acting on behavioral rather than on life-history traits per se can be expected in all fisheries that operate with passive gears such as trapping, angling and gill-netting. Recent artificial selection experiments in the nest-guarding largemouth bass Micropterus salmoides suggest that fishing-induced evolution of behavioral traits that reduce exposure to fishing gear might be maladaptive, potentially reducing natural recruitment. To improve understanding and management of fisheries-induced evolution, we encourage greater application of methods from behavioral ecology, physiological ecology and behavioral genetics.     

Pleiotropy or linkage? Their relative contributions to the genetic correlation of quantitative traits and detection by multitrait GWA studies

Genetic correlations between traits may cause correlated responses to selection. Previous models described the conditions under which genetic correlations are expected to be maintained. Selection, mutation, and migration are all proposed to affect genetic correlations, regardless of whether the underlying genetic architecture consists of pleiotropic or tightly linked loci affecting the traits. Here, we investigate the conditions under which pleiotropy and linkage have different effects on the genetic correlations between traits by explicitly modeling multiple genetic architectures to look at the effects of selection strength, degree of correlational selection, mutation rate, mutational variance, recombination rate, and migration rate. We show that at mutation-selection(-migration) balance, mutation rates differentially affect the equilibrium levels of genetic correlation when architectures are composed of pairs of physically linked loci compared to architectures of pleiotropic loci. Even when there is perfect linkage (no recombination within pairs of linked loci), a lower genetic correlation is maintained than with pleiotropy, with a lower mutation rate leading to a larger decrease. These results imply that the detection of causal loci in multitrait association studies will be affected by the type of underlying architectures, whereby pleiotropic variants are more likely to be underlying multiple detected associations. We also confirm that tighter linkage between nonpleiotropic causal loci maintains higher genetic correlations at the traits and leads to a greater proportion of false positives in association analyses.     

Characterizing the evolution of genetic variance using genetic covariance tensors

Determining how genetic variance changes under selection in natural populations has proved to be a very resilient problem in evolutionary genetics. In the same way that understanding the availability of genetic variance within populations requires the simultaneous consideration of genetic variance in sets of functionally related traits, determining how genetic variance changes under selection in natural populations will require ascertaining how genetic variance–covariance (G) matrices evolve. Here, we develop a geometric framework using higher-order tensors, which enables the empirical characterization of how G matrices have diverged among populations. We then show how divergence among populations in genetic covariance structure can then be associated with divergence in selection acting on those traits using key equations from evolutionary theory. Using estimates of G matrices of eight male sexually selected traits from nine geographical populations of Drosophila serrata, we show that much of the divergence in genetic variance occurred in a single trait combination, a conclusion that could not have been reached by examining variation among the individual elements of the nine G matrices. Divergence in G was primarily in the direction of the major axes of genetic variance within populations, suggesting that genetic drift may be a major cause of divergence in genetic variance among these populations.