Drift on holey landscapes as a dominant evolutionary process.

An organism's phenotype has been shaped by evolution but the specific processes have to be indirectly inferred for most species. For example, correlations among traits imply the historical action of correlated selection and, more generally, the expression and distribution of traits is expected to be reflective of the adaptive landscapes that have shaped a population. However, our expectations about how quantitative traits-like most behaviors, physiological processes, and life-history traits-should be distributed under different evolutionary processes are not clear. Here, we show that genetic variation in quantitative traits is not distributed as would be expected under dominant evolutionary models. Instead, we found that genetic variation in quantitative traits across six phyla and 60 species (including both Plantae and Animalia) is consistent with evolution across high-dimensional "holey landscapes." This suggests that the leading conceptualizations and modeling of the evolution of trait integration fail to capture how phenotypes are shaped and that traits are integrated in a manner contrary to predictions of dominant evolutionary theory. Our results demonstrate that our understanding of how evolution has shaped phenotypes remains incomplete and these results provide a starting point for reassessing the relevance of existing evolutionary models.

A method to predict the response to directional selection using a Kalman filter.

Predicting evolution remains challenging. The field of quantitative genetics provides predictions for the response to directional selection through the breeder's equation, but these predictions can have errors. The sources of these errors include omission of traits under selection, inaccurate estimates of genetic variance, and nonlinearities in the relationship between genetic and phenotypic variation. Previous research showed that the expected value of these prediction errors is often not zero, so predictions are systematically biased. Here, we propose that this bias, rather than being a nuisance, can be used to improve the predictions. We use this to develop a method to predict evolution, which is built on three key innovations. First, the method predicts change as the breeder's equation plus a bias term. Second, the method combines information from the breeder's equation and from the record of past changes in the mean to predict change using a Kalman filter. Third, the parameters of the filter are fitted in each generation using a learning algorithm on the record of past changes. We compare the method to the breeder's equation in two artificial selection experiments, one using the wing of the fruit fly and another using simulations that include a complex mapping of genotypes to phenotypes. The proposed method outperforms the breeder's equation, particularly when traits under selection are omitted from the analysis, when data are noisy, and when additive genetic variance is estimated inaccurately or not estimated at all. The proposed method is easy to apply, requiring only the trait means over past generations.

Effect of the Seed Bank on Evolutionary Rescue in Small Populations: Univariate and Multivariate Demogenetic Dynamics.

AbstractUnder global change, the impact of seed banks on evolutionary rescue is uncertain. They buffer plant populations from demographic and genetic stochasticity but extend generation time and can become a reservoir of maladapted alleles. We built analytical and individual-based models to predict the effect of seed banks on the persistence of small annual plant populations facing an abrupt or sustained directional change in uni- or multivariate trait optima. Demogenetic dynamics predict that under most scenarios seed banks increase the lag yet enhance persistence to 200-250 years by absorbing demographic losses. Simulations indicate that the seed bank has a minimal impact on the genetic skew, although we suggest that this result could depend on the fitness component under selection. Our multivariate model reveals that by enlarging and reshaping the G matrix, seed banks can diminish the impact of mutational correlation and even accelerate adaptation under antagonistic pleiotropy relative to populations without a bank. We illustrate how the magnitude of optimum fluctuations, type and degree of optimum change, selection strength, and vital rates are weights that tip the scales determining persistence. Finally, our work highlights that migration from the past is not maladaptative when optimum fluctuations are large enough to create stepping stones to the new optimum.

Evolutionary potential under heat and drought stress at the southern range edge of North American Arabidopsis lyrata.

The warm edges of species' distributions are vulnerable to global warming. Evidence is the recent range retraction from there found in many species. It is unclear why populations cannot easily adapt to warmer, drier, or combined hot and dry conditions and locally persist. Here, we assessed the ability to adapt to these stressors in the temperate species Arabidopsis lyrata. We grew plants from replicate seed families of a central population with high genetic diversity under a temperature and precipitation regime typical of the low-latitude margin or under hotter and/or drier conditions within naturally occurring amplitudes. We then estimated genetic variance-covariance (G-) matrices of traits depicting growth and allocation as well as selection vectors to compare the predicted adaptation potential under the different climate-stress regimes. We found that the sum of genetic variances and genetic correlations were not significantly different under stress as compared to benign conditions. However, under drought and heat drought, the predicted ability to adapt was severely constrained due to strong selection and selection pointing in a direction with less multivariate genetic variation. The much-reduced ability to adapt to dry and hot-dry conditions is likely to reduce the persistence of populations at the low-latitude margin of the species' distribution and contribute to the local extinction of the species under further warming.

Experimental Evidence That Phenotypic Evolution but Not Plasticity Occurs along Genetic Lines of Least Resistance in Homogeneous Environments.

AbstractGenetic correlations concentrate genetic variation in certain directions of the multivariate phenotype. Adaptation and, under some models, plasticity is expected to occur in the direction of the phenotype containing the greatest amount of genetic variation (gmax). However, this may hinge on environmental heterogeneity, which can affect patterns of genetic variation. I use experimental evolution to test whether plasticity and phenotypic evolution follow gmax during adaptation to environments that varied in environmental heterogeneity. For >25 generations, Drosophila melanogaster populations were exposed to six homogeneous or spatially and temporally heterogeneous treatments involving hot (25°C) and cold (16°C) temperatures. Five wing traits were assayed in both temperatures. Wing morphology diverged between populations evolving in homogeneous hot and cold temperatures in a direction of the phenotype containing a large proportion of genetic variance and that aligned closely with gmax at 16°C but not at 25°C. Spatial heterogeneity produced an intermediate phenotype, which was associated with similar genetic variance across assay temperatures compared with all other treatments. Surprisingly, plasticity across assay temperatures was in a different direction to phenotypic evolution and aligned better with maternal variance than gmax. Together, these results provide experimental evidence for evolution along genetic lines of least resistance in homogeneous environments but no support for predicting plastic responses from the orientation of genetic variation. These results also suggest that spatial heterogeneity could maintain genetic variation that increases the stability of genetic variance across environments.

Eco-Evolutionary Consequences of Dispersal Syndromes during Colonization in a Passerine Bird.

AbstractIn most animal species, dispersing individuals possess phenotypic attributes that mitigate the costs of colonization and/or increase settlement success in new areas (dispersal syndromes). This phenotypic integration likely affects population dynamics and the direction of selection, but data are lacking for natural populations. Using an approach that combines population dynamics, quantitative genetics, and phenotypic selection analyses, we reveal the existence of dispersal syndromes in a pied flycatcher (Ficedula hypoleuca) population in the Netherlands: immigrants were larger, tended to have darker plumage, bred earlier, and produced larger clutches than local recruits, and some of these traits were genetically correlated. Over time, the phenotypic profile of the population gradually changed: each generation advanced arrival and breeding and exhibited longer wings as a result of direct and indirect selection on these correlated traits. Although phenotypic attributes of immigrants were favored by selection during the early phase of colonization, observed phenotypic changes were similar for immigrants and local recruits. We propose that immigrants facilitated initial population establishment but that temporal changes likely resulted from climate change-induced large-scale selection. This study highlights that newly established populations are of nonrandom composition and that phenotypic architecture affects evolutionary population trajectories.

Does the definition of a novel environment affect the ability to detect cryptic genetic variation?

Anthropogenic change exposes populations to environments that have been rare or entirely absent from their evolutionary past. Such novel environments are hypothesized to release cryptic genetic variation, a hidden store of variance that can fuel evolution. However, support for this hypothesis is mixed. One possible reason is a lack of clarity in what is meant by 'novel environment', an umbrella term encompassing conditions with potentially contrasting effects on the exposure or concealment of cryptic variation. Here, we use a meta-analysis approach to investigate changes in the total genetic variance of multivariate traits in ancestral versus novel environments. To determine whether the definition of a novel environment could explain the mixed support for a release of cryptic genetic variation, we compared absolute novel environments, those not represented in a population's evolutionary past, to extreme novel environments, those involving frequency or magnitude changes to environments present in a population's ancestry. Despite sufficient statistical power, we detected no broad-scale pattern of increased genetic variance in novel environments, and finding the type of novel environment did not explain any significant variation in effect sizes. When effect sizes were partitioned by experimental design, we found increased genetic variation in studies based on broad-sense measures of variance, and decreased variation in narrow-sense studies, in support of previous research. Therefore, the source of genetic variance, not the definition of a novel environment, was key to understanding environment-dependant genetic variation, highlighting non-additive genetic variance as an important component of cryptic genetic variation and avenue for future research.

Genetic architecture of multiple mutualisms and mating system in Turnera ulmifolia.

Plants often associate with multiple arthropod mutualists. These partners provide important services to their hosts, but multiple interactions can constrain a plant's ability to respond to complex, multivariate selection. Here, we quantified patterns of genetic variance and covariance among rewards for pollination, biotic defence and seed dispersal mutualisms in multiple populations of Turnera ulmifolia to better understand how the genetic architecture of multiple mutualisms might influence their evolution. We phenotyped plants cultivated from 17 Jamaican populations for several mutualism and mating system-related traits. We then fit genetic variance-covariance (G) matrices for the island metapopulation and the five largest individual populations. At the metapopulation level, we observed significant positive genetic correlations among stigma-anther separation, floral nectar production and extrafloral nectar production. These correlations have the potential to significantly constrain or facilitate the evolution of multiple mutualisms in T. ulmifolia and suggest that pollination, seed dispersal and defence mutualisms do not evolve independently. In particular, we found that positive genetic correlations between floral and extrafloral nectar production may help explain their stable coexistence in the face of physiological trade-offs and negative interactions between pollinators and ant bodyguards. Locally, we found only small differences in G among our T. ulmifolia populations, suggesting that geographic variation in G may not shape the evolution of multiple mutualisms.

Predicting the Evolution of Sexual Dimorphism in Gene Expression.

Sexual dimorphism in gene expression is likely to be the underlying source of dimorphism in a variety of traits. Many analyses implicitly make the assumption that dimorphism only evolves when selection favors different phenotypes in the two sexes, although theory makes clear that it can also evolve as an indirect response to other kinds of selection. Furthermore, previous analyses consider the evolution of a single transcript or trait at a time, ignoring the genetic covariance with other transcripts and traits. We first show which aspects of the genetic-variance-covariance matrix, G, affect dimorphism when these assumptions about selection are relaxed. We then reanalyze gene expression data from Drosophila melanogaster with these predictions in mind. Dimorphism of gene expression for individual transcripts shows the signature of both direct selection for dimorphism and indirect responses to selection. To account for the effect of measurement error on evolutionary predictions, we estimated a G matrix for eight linear combinations of expression traits. Sex-specific genetic variances in female- and male-biased transcription, as well as one relatively unbiased combination, were quite unequal, ensuring that most forms of selection on these traits will have large effects on dimorphism. Predictions of response to selection based on the whole G matrix showed that sexually concordant and antagonistic selection are equally capable of changing sexual dimorphism. In addition, the indirect responses of dimorphism due to cross-trait covariances were quite substantial. The assumption that sexual dimorphism in transcription is an adaptation could be incorrect in many specific cases.

Evolution of the G Matrix under Nonlinear Genotype-Phenotype Maps.

AbstractThe G matrix is a statistical summary of the genetic basis of a set of traits and a central pillar of quantitative genetics. A persistent controversy is whether G changes slowly or quickly over time. The evolution of G is important because it affects the ability to predict, or reconstruct, evolution by selection. Empirical studies have found mixed results on how fast G evolves. Theoretical work has largely been developed under the assumption that the relationship between genetic variation and phenotypic variation-the genotype-phenotype map (GPM)-is linear. Under this assumption, G is expected to remain constant over long periods of time. However, according to developmental biology, the GPM is typically complex and nonlinear. Here, we use a GPM model based on the development of a multicellular organ to study how G evolves. We find that G can change relatively fast and in qualitative different ways, which we describe in detail. Changes can be particularly large when the population crosses between regions of the GPM that have different properties. This can result in the additive genetic variance in the direction of selection fluctuating over time and even increasing despite the eroding effect of selection.

Conservation and Convergence of Genetic Architecture in the Adaptive Radiation of Anolis Lizards.

AbstractThe G matrix, which quantifies the genetic architecture of traits, is often viewed as an evolutionary constraint. However, G can evolve in response to selection and may also be viewed as a product of adaptive evolution. Convergent evolution of G in similar environments would suggest that G evolves adaptively, but it is difficult to disentangle such effects from phylogeny. Here, we use the adaptive radiation of Anolis lizards to ask whether convergence of G accompanies the repeated evolution of habitat specialists, or ecomorphs, across the Greater Antilles. We measured G in seven species representing three ecomorphs (trunk-crown, trunk-ground, and grass-bush). We found that the overall structure of G does not converge. Instead, the structure of G is well conserved and displays a phylogenetic signal consistent with Brownian motion. However, several elements of G showed signatures of convergence, indicating that some aspects of genetic architecture have been shaped by selection. Most notably, genetic correlations between limb traits and body traits were weaker in long-legged trunk-ground species, suggesting effects of recurrent selection on limb length. Our results demonstrate that common selection pressures may have subtle but consistent effects on the evolution of G, even as its overall structure remains conserved.

Axes of multivariate sexual signal divergence among incipient species: Concordance with selection, genetic variation and phenotypic plasticity.

Sexual signalling traits are often observed to diverge rapidly among populations, thereby playing a potentially key early role in the evolution of reproductive isolation. While often assumed to reflect divergent sexual selection among populations, patterns of sexual trait diversification might sometimes be biased along axes of standing additive genetic variation and covariation among trait components. Additionally, theory predicts that environmentally induced phenotypic variation might facilitate rapid trait evolution, suggesting that patterns of divergence between populations should mirror phenotypic plasticity within populations. Here, we evaluate the concordance between observed axes of multivariate sexual trait divergence and predicted divergence based on (1) interpopulation variation in sexual selection, (2) additive genetic variances and (3) temperature-related phenotypic plasticity in male courtship song among geographically isolated populations of the Hawaiian swordtail cricket, Laupala cerasina, which exhibit sexual isolation due acoustic signalling traits. The major axis of multivariate divergence, dmax , accounted for 76% of variation among population male song trait means and was moderately correlated with interpopulation differences in directional sexual selection based on female preferences. However, the majority of additive genetic variance was largely oriented away from the direction of divergence, suggesting that standing genetic variation may not play a dominant role in the patterning of signal divergence. In contrast, the axis of phenotypic plasticity strongly mirrored patterns of interpopulation phenotypic divergence, which is consistent with a role for temperature-related plasticity in facilitating instead of inhibiting male song evolution and sexual isolation in these incipient species. We propose potential mechanisms by which sexual selection might interact with phenotypic plasticity to facilitate the rapid acoustic diversification observed in this species and clade.

Environmental effects on the genetic architecture of fitness components in a simultaneous hermaphrodite.

Understanding how environmental change affects genetic variances and covariances of reproductive traits is key to formulate firm predictions on evolutionary responses. This is particularly true for sex-specific variance in reproductive success, which has been argued to affect how populations can adapt to environmental change. Our current knowledge on the impact of environmental stress on sex-specific genetic architecture of fitness components is still limited and restricted to separate-sexed organisms. However, hermaphroditism is widespread across animals and may entail interesting peculiarities with respect to genetic constraints imposed on the evolution of male and female reproduction. We explored how food restriction affects the genetic variance-covariance (G) matrix of body size and reproductive success of the simultaneously hermaphroditic freshwater snail Physa acuta. Our results provide strong evidence that the imposed environmental stress elevated the opportunity for selection in both sex functions. However, the G-matrix remained largely stable across the tested food treatments. Importantly, our results provide no support for cross-sex genetic correlations suggesting no strong evolutionary coupling of male and female reproductive traits. We discuss potential implications for the adaptation to changing environments and highlight the need for more quantitative genetic studies on male and female fitness components in simultaneous hermaphrodites.

Water and nutrient availability exert selection on reproductive phenology.

PREMISE: Global change has changed resource availability to plants, which could shift the adaptive landscape. We hypothesize that novel water and nutrient availability combinations alter patterns of natural selection on reproductive phenology in Boechera stricta (Brassicaceae) and influence the evolution of local adaptation. METHODS: We conducted a multifactorial greenhouse study using 35 accessions of B. stricta sourced from a broad elevational gradient in the Rocky Mountains. We exposed full siblings to three soil water and two nutrient availability treatment levels, reflecting current and projected future conditions. In addition, we quantified fitness (seed count) and four phenological traits: the timing of first flowering, the duration of flowering, and height and leaf number at flowering. RESULTS: Selection favored early flowering and longer duration of flowering, and the genetic correlation between these traits accorded with the direction of selection. In most treatments, we found selection for increased height, but selection on leaf number depended on water availability, with selection favoring more leaves in well-watered conditions and fewer leaves under severe drought. Low-elevation genotypes had the greatest fitness under drought stress, consistent with local adaptation. CONCLUSIONS: We found evidence of strong selection on these heritable traits. Furthermore, the direction and strength of selection on size at flowering depended on the variable measured (height vs. leaf number). Finally, selection often favored both early flowering and a longer duration of flowering. Selection on these two components of phenology can be difficult to disentangle due to tight genetic correlations.

The genetic architecture of sexual dimorphism in the moss Ceratodon purpureus.

A central problem in evolutionary biology is to identify the forces that maintain genetic variation for fitness in natural populations. Sexual antagonism, in which selection favours different variants in males and females, can slow the transit of a polymorphism through a population or can actively maintain fitness variation. The amount of sexually antagonistic variation to be expected depends in part on the genetic architecture of sexual dimorphism, about which we know relatively little. Here, we used a multivariate quantitative genetic approach to examine the genetic architecture of sexual dimorphism in a scent-based fertilization syndrome of the moss Ceratodon purpureus. We found sexual dimorphism in numerous traits, consistent with a history of sexually antagonistic selection. The cross-sex genetic correlations (rmf) were generally heterogeneous with many values indistinguishable from zero, which typically suggests that genetic constraints do not limit the response to sexually antagonistic selection. However, we detected no differentiation between the female- and male-specific trait (co)variance matrices (Gf and Gm, respectively), meaning the evolution of sexual dimorphism may be constrained. The cross-sex cross-trait covariance matrix B contained both symmetric and asymmetric elements, indicating that the response to sexually antagonistic or sexually concordant selection, and the constraint to sexual dimorphism, are highly dependent on the traits experiencing selection. The patterns of genetic variances and covariances among these fitness components is consistent with partly sex-specific genetic architectures having evolved in order to partially resolve multivariate genetic constraints (i.e. sexual conflict), enabling the sexes to evolve towards their sex-specific multivariate trait optima.

Sex-specific genetic (co)variances of standard metabolic rate, body mass and locomotor activity in Drosophila melanogaster.

A longstanding focus in evolutionary physiology concerns the causes and consequences of variation in maintenance metabolism. Insight into this can be gained by estimating the sex-specific genetic architecture of maintenance metabolism alongside other, potentially correlated traits on which selection may also act, such as body mass and locomotor activity. This may reveal potential genetic constraints affecting the evolution of maintenance metabolism. Here, we used a half-sibling breeding design to quantify the sex-specific patterns of genetic (co)variance in standard metabolic rate (SMR), body mass and daily locomotor activity in Drosophila melanogaster. There was detectable additive genetic variance for all traits in both sexes. As expected, SMR and body mass were strongly and positively correlated, with genetic allometry exponents (bA  ± SE) that were close to 2/3 in females (0.66 ± 0.16) and males (0.58 ± 0.32). There was a significant and positive genetic correlation between SMR and locomotor activity in males, suggesting that alleles that increase locomotion have pleiotropic effects on SMR. Sexual differences in the genetic architecture were largely driven by a difference in genetic variance in locomotor activity between the sexes. Overall, genetic variation was mostly shared between males and females, setting the stage for a potential intralocus sexual conflict in the face of sexually antagonistic selection.

Floral signals evolve in a predictable way under artificial and pollinator selection in Brassica rapa.

BACKGROUND: Angiosperms employ an astonishing variety of visual and olfactory floral signals that are generally thought to evolve under natural selection. Those morphological and chemical traits can form highly correlated sets of traits. It is not always clear which of these are used by pollinators as primary targets of selection and which would be indirectly selected by being linked to those primary targets. Quantitative genetics tools for predicting multiple traits response to selection have been developed since long and have advanced our understanding of evolution of genetically correlated traits in various biological systems. We use these tools to predict the evolutionary trajectories of floral traits and understand the selection pressures acting on them. RESULTS: We used data from an artificial selection and a pollinator (bumblebee, hoverfly) evolution experiment with fast cycling Brassica rapa plants to predict evolutionary changes of 12 floral volatiles and 4 morphological floral traits in response to selection. Using the observed selection gradients and the genetic variance-covariance matrix (G-matrix) of the traits, we showed that the observed responses of most floral traits including volatiles were predicted in the right direction in both artificial- and bumblebee-selection experiment. Genetic covariance had a mix of constraining and facilitating effects on evolutionary responses. We further revealed that G-matrices also evolved in the selection processes. CONCLUSIONS: Overall, our integrative study shows that floral signals, especially volatiles, evolve under selection in a mostly predictable way, at least during short term evolution. Evolutionary constraints stemming from genetic covariance affected traits evolutionary trajectories and thus it is important to include genetic covariance for predicting the evolutionary changes of a comprehensive suite of traits. Other processes such as resource limitation and selfing also need to be considered for a better understanding of floral trait evolution.

Non-consumptive effects of predation: does perceived risk strengthen the genetic integration of behaviour and morphology in stickleback?

Predators can shape genetic correlations in prey by altering prey perception of risk. We manipulated perceived risk to test whether such non-consumptive effects tightened behavioural trait correlations in wild-caught stickleback from high- compared to low-risk environments due to genetic variation in plasticity. We expected tighter genetic correlations within perceived risk treatments than across them, and tighter genetic correlations in high-risk than in low-risk treatments. We identified genetic variation in plasticity, with genetic correlations between boldness, sociality, and antipredator morphology, as expected, being tighter within treatments than across them, for both of two populations. By contrast, genetic correlations did not tighten with exposure to risk. Tighter phenotypic correlations in wild stickleback may thus arise because predators induce correlational selection on environmental components of these traits, or because predators tighten residual correlations by causing environmental heterogeneity that is controlled in the laboratory. Our study places phenotypic integration firmly into an ecological context.

Demography-Dispersal Trait Correlations Modify the Eco-Evolutionary Dynamics of Range Expansion.

Spreading populations are subject to evolutionary processes acting on dispersal and reproduction that can increase invasion speed and variability. It is typically assumed that dispersal and demography traits evolve independently, but abundant evidence points to correlations between them that may be positive or negative and genetic, maternal, or environmental. We sought to understand how demography-dispersal correlations modify the eco-evolutionary dynamics of range expansion. We first explored this question with the beetle Callosobruchus maculatus, a laboratory model in which evolutionary acceleration of invasion has been demonstrated. We then built a simulation model to explore the role of trait correlations in this system and more generally. We found that positive correlations amplify the positive influence of evolution on speed and variability while negative correlations (such as we found empirically) constrain that influence. Strong negative genetic correlations can even cause evolution to decelerate invasion. Genetic and nongenetic (maternal and environmental) correlations had similar effects on some measures of invasion but different effects on others. Model results enabled us to retrospectively explain invasion dynamics and trait evolution in C. maculatus and may similarly aid the interpretation of other field and laboratory studies. Nonindependence of demography and dispersal is an important consideration for understanding and predicting outcomes of range expansion.

Predicting Multivariate Responses of Sexual Dimorphism to Direct and Indirect Selection.

AbstractSexual dimorphism is often assumed to result from balancing the strength of antagonistic selection in favor of dimorphism against the degree of constraint imposed by the shared genome of the sexes, reflected in the B matrix of genetic intersexual covariances. To investigate the totality of forces shaping dimorphism, we reparameterized the Lande equation to predict changes in trait averages and trait differences between the sexes. As genetic constraints on the evolution of dimorphism in response to antagonistic selection become larger, dimorphism will tend to respond more rapidly to concordant selection (which favors the same direction of change in male and female traits) than to antagonistic selection. When we apply this theory to four empirical estimates of B in Drosophila melanogaster, the indirect responses of dimorphism to concordant selection are of comparable or larger magnitude than the direct responses of dimorphism to antagonistic selection in two suites of traits with typical levels of intersex correlation. Antagonistic selection is more important in two suites of traits where the intersex correlations are unusually low. This suggests that the evolution of sexual dimorphism may sometimes be dominated by concordant selection rather than antagonistic selection.