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.

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.

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.

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.

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.

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.

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.

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.

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.

Complex constraints on allometry revealed by artificial selection on the wing of Drosophila melanogaster.

Precise exponential scaling with size is a fundamental aspect of phenotypic variation. These allometric power laws are often invariant across taxa and have long been hypothesized to reflect developmental constraints. Here we test this hypothesis by investigating the evolutionary potential of an allometric scaling relationship in drosophilid wing shape that is nearly invariant across 111 species separated by at least 50 million years of evolution. In only 26 generations of artificial selection in a population of Drosophila melanogaster, we were able to drive the allometric slope to the outer range of those found among the 111 sampled species. This response was rapidly lost when selection was suspended. Only a small proportion of this reversal could be explained by breakup of linkage disequilibrium, and direct selection on wing shape is also unlikely to explain the reversal, because the more divergent wing shapes produced by selection on the allometric intercept did not revert. We hypothesize that the reversal was instead caused by internal selection arising from pleiotropic links to unknown traits. Our results also suggest that the observed selection response in the allometric slope was due to a component expressed late in larval development and that variation in earlier development did not respond to selection. Together, these results are consistent with a role for pleiotropic constraints in explaining the remarkable evolutionary stability of allometric scaling.

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).

Euglossine bees mediate only limited long-distance gene flow in a tropical vine.

Euglossine bees (Apidae: Euglossini) have long been hypothesized to act as long-distance pollinators of many low-density tropical plants. We tested this hypothesis by the analysis of gene flow and genetic structure within and among populations of the euglossine bee-pollinated vine Dalechampia scandens. Using microsatellite markers, we assessed historical gene flow by the quantification of regional-scale genetic structure and isolation by distance among 18 populations, and contemporary gene flow by the estimation of recent migration rates among populations. To assess bee-mediated pollen dispersal on a smaller scale, we conducted paternity analyses within a focal population, and quantified within-population spatial genetic structure in four populations. Gene flow was limited to certain nearby populations within continuous forest blocks, whereas drift appeared to dominate on larger scales. Limited long-distance gene flow was supported by within-population patterns; gene flow was biased towards nearby plants, and significant small-scale spatial genetic structure was detected within populations. These findings suggest that, although female euglossine bees might be effective at moving pollen within populations, and perhaps within forest blocks, their contribution to gene flow on the regional scale seems too limited to counteract genetic drift in patchily distributed tropical plants. Among-population gene flow might have been reduced following habitat fragmentation.

Evolutionary consequences of ecological factors: pollinator reliability predicts mating-system traits of a perennial plant.

The reproductive-assurance hypothesis predicts that mating-system traits will evolve towards increased autonomous self-pollination in plant populations experiencing unreliable pollinator service. We tested this long-standing hypothesis by assessing geographic covariation among pollinator reliability, outcrossing rates, heterozygosity and relevant floral traits across populations of Dalechampia scandens in Costa Rica. Mean outcrossing rates ranged from 0.16 to 0.49 across four populations, and covaried with the average rates of pollen arrival on stigmas, a measure of pollinator reliability. Across populations, genetically based differences in herkogamy (anther-stigma distance) were associated with variation in stigmatic pollen loads, outcrossing rates and heterozygosity. These observations are consistent with the hypothesis that, when pollinators are unreliable, floral traits promoting autonomous selfing evolve as a mechanism of reproductive assurance. Extensive covariation between floral traits and mating system among closely related populations further suggests that floral traits influencing mating systems track variation in adaptive optima generated by variation in pollinator reliability.

Does stronger pollen competition improve offspring fitness when pollen load does not vary?

PREMISE OF THE STUDY: Competition among pollen grains from a single donor is expected to increase the quality of the offspring produced because of the recessive deleterious alleles expressed during pollen-tube growth. However, evidence for such an effect is inconclusive; a large number of studies suffer from confounding variation in pollen competition with variation in pollen load. METHODS: In this study, we tested the effect of pollen competition on offspring performance independently of pollen-load variation. We compared seed mass and early seedling performance in Dalechampia scandens (Euphorbiaceae) between crosses in which variation in pollen competition was achieved, without variation in pollen load, by manipulating the dispersion of pollen grains on the stigmas. KEY RESULTS: Despite a large sample size (211 crosses on 20 maternal plants), we failed to find an effect of pollen competition on seed characteristics or early seedling performance. Paternal effects were always limited, and pollen competition never reduced the within-father (residual) variance. CONCLUSION: These results suggest that limited within-donor variation in genetic quality of pollen grains reduces the potential benefits of pollen competition in the study population. The lack of paternal effects on early sporophyte performance further suggests that benefits of pollen competition among pollen from multiple donors should be limited as well, and it raises questions about the significance of pollen competition as a mechanism of sexual selection.

On The Importance Of Scale In Evolutionary Quantitative Genetics.

The informed use of scales and units in evolutionary quantitative genetics is often neglected, and naïve standardizations can cause misinterpretations of empirical results. A potentially influential example of such neglect can be found in the recent book by Stevan J. Arnold (2023. Evolutionary Quantitative Genetics Oxford University Press). There, Arnold championed the use of heritability over mean-scaled genetic variance as a measure of evolutionary potential arguing that mean-scaled genetic variances are correlated with trait means while heritabilities are not. Here, we show that Arnold's empirical result is an artifact of ignoring the units in which traits are measured. More importantly, Arnold's argument mistakenly assumes that the goal of mean scaling is to remove the relationship between mean and variance. In our view, the purpose of mean scaling is to put traits with different units on a common scale that makes evolutionary changes, or their potential, readily interpretable and comparable in terms of proportions of the mean.

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 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.

On the relationship between ontogenetic and static allometry.

Ontogenetic and static allometries describe how a character changes in size when the size of the organism changes during ontogeny and among individuals measured at the same developmental stage, respectively. Understanding the relationship between these two types of allometry is crucial to understanding the evolution of allometry and, more generally, the evolution of shape. However, the effects of ontogenetic allometry on static allometry remain largely unexplored. Here, we first show analytically how individual variation in ontogenetic allometry and body size affect static allometry. Using two longitudinal data sets on ontogenetic and static allometry, we then estimate variances and covariances for the different parameters of the ontogenetic allometry defined in our model and assess their relative contribution to the static allometric slope. The mean ontogenetic allometry is the main parameter that determines the static allometric slope, while the covariance between the ontogenetic allometric slope and body size generates most of the discrepancies between ontogenetic and static allometry. These results suggest that the apparent evolutionary stasis of the static allometric slope is not generated by internal (developmental) constraints but more likely results from external constraints imposed by selection.

Decoupled phenotypic variation between floral and vegetative traits: distinguishing between developmental and environmental correlations.

BACKGROUND AND AIMS: In species with specialized pollination, floral traits are expected to be relatively invariant and decoupled from the phenotypic variation affecting vegetative traits. However, inferring the degree of decoupling between morphological characters from patterns of phenotypic correlations is difficult because phenotypic correlations result from the superimposition of several sources of covariance. In this study it is hypothesized that, in some cases, negative environmental correlations generated by non-congruent reaction norms across traits overshadow positive developmental correlations and generate a decoupling of the phenotypic variation between vegetative and floral traits. METHODS: To test this hypothesis, Campanula rotundifolia were grown from two distinct populations under two temperature treatments, and patterns of correlation were analysed between leaf size and flower size within and among treatments. KEY RESULTS: Flower size was less sensitive to temperature variation than leaf size. Furthermore, flower size and leaf size showed temperature-induced reaction norms in opposite directions. Flower size decreased with an increasing temperature, while leaf size increased. Consequently, among treatments, correlations between leaf size and flower size were negative or absent, while, within treatments, these correlations were positive or absent in the cold and warm environments, respectively. CONCLUSIONS: These results confirm that the decoupling of the phenotypic variation between vegetative and floral traits can be dependent on the environment. They also underline the importance of distinguishing sources of phenotypic covariance when testing hypotheses about phenotypic integration.