Evolvability predicts macroevolution under fluctuating selection.

Heritable variation is a prerequisite for evolutionary change, but the relevance of genetic constraints on macroevolutionary timescales is debated. By using two datasets on fossil and contemporary taxa, we show that evolutionary divergence among populations, and to a lesser extent among species, increases with microevolutionary evolvability. We evaluate and reject several hypotheses to explain this relationship and propose that an effect of evolvability on population and species divergence can be explained by the influence of genetic constraints on the ability of populations to track rapid, stationary environmental fluctuations.

Directional epistasis is common in morphological divergence.

Epistasis is often portrayed as unimportant in evolution. While random patterns of epistasis may have limited effects on the response to selection, systematic directional epistasis can have substantial effects on evolutionary dynamics. Directional epistasis occurs when allele substitutions that change a trait also modify the effects of allele substitution at other loci in a systematic direction. In this case, trait evolution may induce correlated changes in allelic effects and additive genetic variance (evolvability) that modify further evolution. Although theory thus suggests a potentially important role for directional epistasis in evolution, we still lack empirical evidence about its prevalence and magnitude. Using a new framework to estimate systematic patterns of epistasis from line-crosses experiments, we quantify its effects on 197 size-related traits from diverging natural populations in 24 animal and 17 plant species. We show that directional epistasis is common and tends to become stronger with increasing morphological divergence. In animals, most traits displayed negative directionality toward larger size, suggesting that epistatic constraints reducing evolvability toward larger size. Dominance was also common but did not systematically alter the effects of epistasis.

Evolvability and trait function predict phenotypic divergence of plant populations.

Understanding the causes and limits of population divergence in phenotypic traits is a fundamental aim of evolutionary biology, with the potential to yield predictions of adaptation to environmental change. Reciprocal transplant experiments and the evaluation of optimality models suggest that local adaptation is common but not universal, and some studies suggest that trait divergence is highly constrained by genetic variances and covariances of complex phenotypes. We analyze a large database of population divergence in plants and evaluate whether evolutionary divergence scales positively with standing genetic variation within populations (evolvability), as expected if genetic constraints are evolutionarily important. We further evaluate differences in divergence and evolvability-divergence relationships between reproductive and vegetative traits and between selfing, mixed-mating, and outcrossing species, as these factors are expected to influence both patterns of selection and evolutionary potentials. Evolutionary divergence scaled positively with evolvability. Furthermore, trait divergence was greater for vegetative traits than for floral (reproductive) traits, but largely independent of the mating system. Jointly, these factors explained ~40% of the variance in evolutionary divergence. The consistency of the evolvability-divergence relationships across diverse species suggests substantial predictability of trait divergence. The results are also consistent with genetic constraints playing a role in evolutionary divergence.

Inferring temperature adaptation from thermal performance curves of somatic growth rate: The importance of growth measurements and mortality.

When comparing somatic growth thermal performance curves (TPCs), higher somatic growth across experimental temperatures is often observed for populations originating from colder environments. Such countergradient variation has been suggested to represent adaptation to seasonality, or shorter favourable seasons in colder climates. Alternatively, populations from cold climates may outgrow those from warmer climates at low temperature, and vice versa at high temperature, representing adaptation to temperature. Using modelling, we show that distinguishing between these two types of adaptation based on TPCs requires knowledge about (i) the relationship between somatic growth rate and population growth rate, which in turn depends on the scale of somatic growth (absolute or proportional), and (ii) the relationship between somatic growth rate and mortality rate in the wild. We illustrate this by quantifying somatic growth rate TPCs for three populations of Daphnia magna where population growth scales linearly with proportional somatic growth. For absolute somatic growth, the northern population outperformed the two more southern populations across temperatures, and more so at higher temperatures, consistent with adaptation to seasonality. In contrast, for the proportional somatic growth TPCs, and hence population growth rate, TPCs tended to converge towards the highest temperatures. Thus, if the northern population pays an ecological mortality cost of rapid growth in the wild, this may create crossing population growth TPCs consistent with adaptation to temperature. Future studies within this field should be more explicit in how they extrapolate from somatic growth in the lab to fitness in the wild.

Quantitative assessment of observed versus predicted responses to selection.

Although artificial-selection experiments seem well suited to testing our ability to predict evolution, the correspondence between predicted and observed responses is often ambiguous due to the lack of uncertainty estimates. We present equations for assessing prediction error in direct and indirect responses to selection that integrate uncertainty in genetic parameters used for prediction and sampling effects during selection. Using these, we analyzed a selection experiment on floral traits replicated in two taxa of the Dalechampia scandens (Euphorbiaceae) species complex for which G-matrices were obtained from a diallel breeding design. After four episodes of bidirectional selection, direct and indirect responses remained within wide prediction intervals, but appeared different from the predictions. Combined analyses with structural-equation models confirmed that responses were asymmetrical and lower than predicted in both species. We show that genetic drift is likely to be a dominant source of uncertainty in typically-dimensioned selection experiments in plants and a major obstacle to predicting short-term evolutionary trajectories.

Using ecological context to interpret spatiotemporal variation in natural selection.

Spatiotemporal variation in natural selection is expected, but difficult to estimate. Pollinator-mediated selection on floral traits provides a good system for understanding and linking variation in selection to differences in ecological context. We studied pollinator-mediated selection in five populations of Dalechampia scandens (Euphorbiaceae) in Costa Rica and Mexico. Using a nonlinear path-analytical approach, we assessed several functional components of selection, and linked variation in pollinator-mediated selection across time and space to variation in pollinator assemblages. After correcting for estimation error, we detected moderate variation in net selection on two out of four blossom traits. Both the opportunity for selection and the mean strength of selection decreased with increasing reliability of cross-pollination. Selection for pollinator attraction was consistently positive and stronger on advertisement than reward traits. Selection on traits affecting pollen transfer from the pollinator to the stigmas was strong only when cross-pollination was unreliable and there was a mismatch between pollinator and blossom size. These results illustrate how consideration of trait function and ecological context can facilitate both the detection and the causal understanding of spatiotemporal variation in natural selection.

Low potential for evolutionary rescue from climate change in a tropical fish.

Climate change is increasing global temperatures and intensifying the frequency and severity of extreme heat waves. How organisms will cope with these changes depends on their inherent thermal tolerance, acclimation capacity, and ability for evolutionary adaptation. Yet, the potential for adaptation of upper thermal tolerance in vertebrates is largely unknown. We artificially selected offspring from wild-caught zebrafish (Danio rerio) to increase (Up-selected) or decrease (Down-selected) upper thermal tolerance over six generations. Selection to increase upper thermal tolerance was also performed on warm-acclimated fish to test whether plasticity in the form of inducible warm tolerance also evolved. Upper thermal tolerance responded to selection in the predicted directions. However, compared to the control lines, the response was stronger in the Down-selected than in the Up-selected lines in which evolution toward higher upper thermal tolerance was slow (0.04 ± 0.008 °C per generation). Furthermore, the scope for plasticity resulting from warm acclimation decreased in the Up-selected lines. These results suggest the existence of a hard limit in upper thermal tolerance. Considering the rate at which global temperatures are increasing, the observed rates of adaptation and the possible hard limit in upper thermal tolerance suggest a low potential for evolutionary rescue in tropical fish living at the edge of their thermal limits.

On the use of the coefficient of variation to quantify and compare trait variation.

Meaningful comparison of variation in quantitative trait requires controlling for both the dimension of the varying entity and the dimension of the factor generating variation. Although the coefficient of variation (CV; standard deviation divided by the mean) is often used to measure and compare variation of quantitative traits, it only accounts for the dimension of the former, and its use for comparing variation may sometimes be inappropriate. Here, we discuss the use of the CV to compare measures of evolvability and phenotypic plasticity, two variational properties of quantitative traits. Using a dimensional analysis, we show that contrary to evolvability, phenotypic plasticity cannot be meaningfully compared across traits and environments by mean-scaling trait variation. We further emphasize the need of remaining cognizant of the dimensions of the traits and the relationship between mean and standard deviation when comparing CVs, even when the scales on which traits are expressed allow meaningful calculation of the CV.

Variation in the ontogenetic allometry of horn length in bovids along a body mass continuum.

Allometric relationships describe the proportional covariation between morphological, physiological, or life-history traits and the size of the organisms. Evolutionary allometries estimated among species are expected to result from species differences in ontogenetic allometry, but it remains uncertain whether ontogenetic allometric parameters and particularly the ontogenetic slope can evolve. In bovids, the nonlinear evolutionary allometry between horn length and body mass in males suggests systematic changes in ontogenetic allometry with increasing species body mass. To test this hypothesis, we estimated ontogenetic allometry between horn length and body mass in males and females of 19 bovid species ranging from ca. 5 to 700 kg. Ontogenetic allometry changed systematically with species body mass from steep ontogenetic allometries over a short period of horn growth in small species to shallow allometry with the growth period of horns matching the period of body mass increase in the largest species. Intermediate species displayed steep allometry over long period of horn growth. Females tended to display shallower ontogenetic allometry with longer horn growth compared to males, but these differences were weak and highly variable. These findings show that ontogenetic allometric slope evolved across species possibly as a response to size-related changes in the selection pressures acting on horn length and body mass.

Earlier onset of flowering and increased reproductive allocation of an annual invasive plant in the north of its novel range.

BACKGROUND AND AIMS: It remains unclear whether invasive species can maintain both high biomass and reproductive output across their invaded range. Along latitudinal gradients, allocation theory predicts that faster flowering onset at high latitudes results in maturation at smaller size and thus reduced reproductive output. For annual invasive plants, more favourable environmental conditions at low latitudes probably result in stronger competition of co-occurring species, potentially driving selection for higher investment in vegetative biomass, while harsher climatic conditions and associated reproductive uncertainty at higher latitudes could reduce selection for vegetative biomass and increased selection for high reproductive investment (stress-gradient hypothesis). Combined, these drivers could result in increased or constant reproductive allocation with increasing latitude. METHODS: We quantified life-history traits in the invasive annual plant Impatiens glandulifera along a latitudinal gradient in Europe. By growing two successive glasshouse generations, we assessed genetic differentiation in vegetative growth and reproductive output across six populations, and tested whether onset of flowering drives this divergence. KEY RESULTS: Trait variation was mainly caused by genetic differentiation. As expected, flowering onset was progressively earlier in populations from higher latitudes. Plant height and vegetative biomass also decreased in populations from higher latitudes, as predicted by allocation theory, but their variation was independent of the variation in flowering onset. Reproductive output remained constant across latitudes, resulting in increased reproductive allocation towards higher latitudes, supporting the stress-gradient hypothesis. We also observed trait genetic differentiation among populations that was independent of latitude. CONCLUSIONS: We show that an annual invasive plant evolved several life-history traits across its invaded range in ~150 years. The evolution of vegetative and reproductive traits seems unconstrained by evolution of flowering onset. This genetic decoupling between vegetative and reproductive traits possibly contributes to the invasion success of this species.

The Demographic Buffering Hypothesis: Evidence and Challenges.

In (st)age-structured populations, the long-run population growth rate is negatively affected by temporal variation in vital rates. In most cases, natural selection should minimize temporal variation in the vital rates to which the long-run population growth is most sensitive, resulting in demographic buffering. By reviewing empirical studies on demographic buffering in wild populations, we found overall support for this hypothesis. However, we also identified issues when testing for demographic buffering. In particular, solving scaling problems for decomposing, measuring, and comparing stochastic variation in vital rates and accounting for density dependence are required in future tests of demographic buffering. In the current context of climate change, demographic buffering may mitigate the negative impact of environmental variation and help populations to persist in an increasingly variable environment.

Fitness costs of delayed pollination in a mixed-mating plant.

BACKGROUND AND AIMS: To predict the evolutionary consequences of pollinator declines, we need to understand the evolution of delayed autonomous self-pollination, which is expected to evolve as a mechanism of reproductive assurance when cross-pollination becomes unreliable. This involves estimating the costs of increased levels of selfing as well as those associated with floral senescence. METHODS: We studied the mechanisms and costs of delayed self-pollination in the mixed-mating vine Dalechampia scandens (Euphorbiaceae) by first assessing among-population variation in herkogamy and dichogamy, which together determine the rate and timing of autonomous self-pollination. We then tested whether floral longevity responds plastically to delayed pollination. Finally, we assessed the costs of delayed self-pollination in terms of seed number and size, explicitly separating inbreeding depression from effects of floral senescence. KEY RESULTS: Herkogamy varied extensively, while variation in dichogamy was more limited. Unpollinated blossoms increased their longevity, but seed quantity and quality decreased with increasing delays in pollination, independently of inbreeding depression. CONCLUSIONS: In D. scandens, earlier autonomous selfing is facilitated by reduced herkogamy rather than reduced protogyny, providing reproductive assurance while maintaining the possibility for outcrossing events. Effective early autonomous self-pollination may evolve under reduced cross-pollination reliability in response to costs associated with floral senescence.

Rainfall seasonality predicts the germination behavior of a tropical dry-forest vine.

Seed dormancy is considered to be an adaptive strategy in seasonal and/or unpredictable environments because it prevents germination during climatically favorable periods that are too short for seedling establishment. Tropical dry forests are seasonal environments where seed dormancy may play an important role in plant resilience and resistance to changing precipitation patterns. We studied the germination behavior of seeds from six populations of the Neotropical vine Dalechampia scandens (Euphorbiaceae) originating from environments of contrasting rainfall seasonality. Seeds produced by second greenhouse-generation plants were measured and exposed to a favorable wet environment at different time intervals after capsule dehiscence and seed dispersal. We recorded the success and the timing of germination. All populations produced at least some dormant seeds, but seeds of populations originating from more seasonal environments required longer periods of after-ripening before germinating. Within populations, larger seeds tended to require longer after-ripening periods than did smaller seeds. These results indicate among-population genetic differences in germination behavior and suggest that these populations are adapted to local environmental conditions. They also suggest that seed size may influence germination timing within populations. Ongoing changes in seasonality patterns in tropical dry forests may impose strong selection on these traits.

Genetic and environmental effects on the scaling of metabolic rate with body size.

Metabolic rate (MR) often scales with body mass (BM) following a power function of the form MR=aBM b , where log(a) is the allometric intercept and b is the allometric exponent (i.e. slope on a log-log scale). The variational properties of b have been debated, but very few studies have tested for genetic variance in b, and none have tested for a genotype-by-environment (G×E) interaction in b Consequently, the short-term evolutionary potentials of both b and its phenotypic plasticity remain unknown. Using 10 clones of a population of Daphnia magna, we estimated the genetic variance in b and assessed whether a G×E interaction affected b We measured MR on juveniles of different sizes reared and measured at three temperatures (17, 22 and 28°C). Overall, b decreased with increasing temperature. We found no evidence of genetic variance in b at any temperature, and thus no G×E interaction in b However, we found a significant G×E interaction in size-specific MR. Using simulations, we show how this G×E interaction can generate genetic variation in the ontogenetic allometric slope of animals experiencing directional changes in temperature during growth. This suggests that b can evolve despite having limited genetic variation at constant temperatures.

How to quantify thermal acclimation capacity?

The capacity of organisms to acclimate will influence their ability to cope with ongoing global changes in thermal regimes. Here we highlight methodological issues associated with recent attempts to quantify variation in acclimation capacity among taxa and environments, and describe how these may introduce bias to conclusions. We then propose a measure of thermal acclimation capacity that more directly quantifies the process of acclimation. Future studies of variation in acclimation capacity should critically evaluate whether their chosen empirical metric accurately reflects the theoretical concept of acclimation.

No evidence that seed predators constrain pollinator-mediated trait evolution in a tropical vine.

PREMISE OF THE STUDY: Turnover in biotic communities across heterogeneous landscapes is expected to lead to variation in interactions among plants, their mutualists, and their antagonists. Across a fragmented landscape in northern Costa Rica, populations of the euphorb vine Dalechampia scandens vary widely in mating systems and associated blossom traits. Previous work suggested that populations are well adapted to the local reliability of pollination by apid and megachilid bees. We tested whether variation in the intensity of predispersal seed predation by seed weevils in the genus Nanobaris also contributes to the observed variation in blossom traits. METHODS: We studied spatiotemporal variation in the relationships between floral advertisement and the probability of seed predation within three focal populations. Then we assessed among-population covariation of predation rate, pollination reliability, mating system, and blossom traits across 20 populations. KEY RESULTS: The probability of seed predation was largely unrelated to variation in floral advertisement both within focal populations and among the larger sample of populations. The rate of seed predation was only weakly associated with the rate of cross-pollination (allogamy) in each population but tended to be proportionally greater in populations experiencing less reliable pollination. CONCLUSIONS: These results suggest that geographic variation in the intensity of antagonistic interactions have had only minor modifying effects on the evolutionary trajectories of floral advertisement in plant populations in this system. Thus, pollinator-driven floral trait evolution in D. scandens in the study area appears not to be influenced by conflicting seed-predator-mediated selection.

Quantitative and qualitative consequences of reduced pollen loads in a mixed-mating plant.

Greater pollination intensity can enhance maternal plant fitness by increasing seed set and seed quality as a result of more intense pollen competition or enhanced genetic sampling. We tested experimentally these effects by varying the pollen load from a single pollen donor on stigmas of female flowers of Dalechampia scandens (Euphorbiaceae) and measuring the effects on seed number and seed mass. Seed set increased rapidly with pollen number at low to moderate pollen loads, and a maximum set of three seeds occurred with a mean pollen load of 19 pollen grains. We did not detect a trade-off between the number of seeds and seed mass within a fruit. Seed mass increased with increasing pollen load, supporting the hypothesis of enhanced seed quality via increased pollen-competition intensity or genetic sampling. These results suggest that maternal fitness increases with larger pollen loads, even when the fertilization success is already high. Our results further highlight the importance of high rates of pollen arrival onto stigmas, as mediated by reliable pollinators. Comparing the pollen-to-seed response curve obtained in this experiment with those observed in natural populations suggests that pollen limitation may be more severe in natural populations than predicted from greenhouse studies. These results also indicate that declines in pollinator abundance may decrease plant fitness through lowered seed quality before an effect on seed set is detected.

Intersexual conflict over seed size is stronger in more outcrossed populations of a mixed-mating plant.

In polyandrous species, fathers benefit from attracting greater maternal investment toward their offspring at the expense of the offspring of other males, while mothers should usually allocate resources equally among offspring. This conflict can lead to an evolutionary arms race between the sexes, manifested through antagonistic genes whose expression in offspring depends upon the parent of origin. The arms race may involve an increase in the strength of maternally versus paternally derived alleles engaged in a "tug of war" over maternal provisioning or repeated "recognition-avoidance" coevolution where growth-enhancing paternally derived alleles evolve to escape recognition by maternal genes targeted to suppress their effect. Here, we develop predictions to distinguish between these two mechanisms when considering crosses among populations that have reached different equilibria in this intersexual arms race. We test these predictions using crosses within and among populations of Dalechampia scandens (Euphorbiaceae) that presumably have experienced different intensities of intersexual conflict, as inferred from their historical differences in mating system. In crosses where the paternal population was more outcrossed than the maternal population, hybrid seeds were larger than those normally produced in the maternal population, whereas when the maternal population was more outcrossed, hybrid seeds were smaller than normal. These results confirm the importance of mating systems in determining the intensity of intersexual conflict over maternal investment and provide strong support for a tug-of-war mechanism operating in this conflict. They also yield clear predictions for the fitness consequences of gene flow among populations with different mating histories.

An empirical test for a zone of canalization in thermal reaction norms.

Theoretical models on the evolution of phenotypic plasticity predict a zone of canalization where reaction norms cross, and genetic variation is minimized in the environment a population most frequently encounter. Empirical tests of this prediction are largely missing, in particular for life-history traits. We addressed this prediction by quantifying thermal reaction norms of three life-history traits (somatic growth rate, age and size at maturation) of a Norwegian population of Daphnia magna and testing for the occurrence of an intermediate temperature (Tm ) at which genetic variance in the traits is minimized. Size at maturation changed relatively little with temperature compared to the other traits, and there was no genetic variance in the shape of the reaction norm. Consequently, age at maturation and somatic growth rate were strongly negatively correlated. Both traits showed a strong genotype-environment interaction, and the estimated Tm was 14 °C for both age at maturation and growth rate. This value of Tm corresponds well with mean summer temperatures experienced by the population and suggests that the population has evolved under stabilizing selection in temperatures that fluctuate around this mean temperature. These results suggest local adaptation to temperature in the studied population and allow predicting evolutionary trajectories of thermal reaction norms under changing thermal regimes.

The measure and mismeasure of reciprocity in heterostylous flowers.

The goal of biological measurement is to capture underlying biological phenomena in numerical form. The reciprocity index applied to heterostylous flowers is meant to measure the degree of correspondence between fertile parts of opposite sex on complementary (inter-compatible) morphs, reflecting the correspondence of locations of pollen placement on, and stigma contact with, pollinators. Pollen of typical heterostylous flowers can achieve unimpeded fertilization only on opposite-morph flowers. Thus, the implicit goal of this measurement is to assess the likelihood of 'legitimate' pollinations between compatible morphs, and hence reproductive fitness. Previous reciprocity metrics fall short of this goal on both empirical and theoretical grounds. We propose a new measure of reciprocity based on theory that relates floral morphology to reproductive fitness. This method establishes a scale based on adaptive inaccuracy, a measure of the fitness cost of the deviation of phenotypes in a population from the optimal phenotype. Inaccuracy allows the estimation of independent contributions of maladaptive bias (mean departure from optimum) and imprecision (within-population variance) to the phenotypic mismatch (inaccuracy) of heterostylous morphs on a common scale. We illustrate this measure using data from three species of Primula (Primulaceae).