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Mutations shape genetic architecture and thus influence the evolvability, adaptation and diversification of populations. Mutations may have different and even opposite effects on separate fitness components, and their rate of origin, distribution of effects and variance-covariance structure may depend on environmental quality. We performed an approximately 1,500-generation mutation-accumulation (MA) study in diploids of the yeast Saccharomyces cerevisiae in stressful (high-salt) and normal environments (50 lines each) to investigate the rate of input of mutational variation (Vm) as well as the mutation rate and distribution of effects on diploid and haploid fitness components, assayed in the normal environment. All four fitness components in both MA treatments exhibited statistically significant mutational variance and mutational heritability. Compared to normal-MA, salt stress increased the mutational variance in growth rate by more than sevenfold in haploids derived from the MA lines. This increase was not detected in diploid growth rate, suggesting masking of mutations in the heterozygous state. The genetic architecture arising from mutation (M-matrix) differed between normal and salt conditions. Salt stress also increased environmental variance in three fitness components, consistent with a reduction in canalization. Maximum-likelihood analysis indicated that stress increased the genomic mutation rate by approximately twofold for maximal growth rate and sporulation rate in diploids and for viability in haploids, and by tenfold for maximal growth rate in haploids, but large confidence intervals precluded distinguishing these values between MA environments. We discuss correlations between fitness components in diploids and haploids and compare the correlations between the two MA environmental treatments.

Our understanding of plant biology has been revolutionized by modern genetics and biochemistry. However, biochemical genetics can be traced back to the foundation of Mendelian genetics; indeed, one of Mendel's milestone discoveries of seven characteristics of pea plants later came to be ascribed to a mutation in a starch branching enzyme. Here, we review both current and historical strategies for the elucidation of plant metabolic pathways and the genes that encode their component enzymes and regulators. We use this historical review to discuss a range of classical genetic phenomena including epistasis, canalization, and heterosis as viewed through the lens of contemporary high-throughput data obtained via the array of approaches currently adopted in multiomics studies., (© The Author(s) 2023. Published by Oxford University Press on behalf of the Society for Experimental Biology.)

Most species evolve within fluctuating environments, and have developed adaptations to meet the challenges posed by environmental heterogeneity. One such adaptation is phenotypic plasticity, or the ability of a single genotype to produce multiple environmentally-induced phenotypes. Yet, not all plasticity is adaptive. Despite the renewed interest in adaptive phenotypic plasticity and its consequences for evolution, much less is known about maladaptive plasticity. However, maladaptive plasticity is likely an important driver of phenotypic similarity among populations living in different environments. This paper traces four strategies for overcoming maladaptive plasticity that result in phenotypic similarity, two of which involve genetic changes (standing genetic variation, genetic compensation) and two of which do not (standing epigenetic variation, plastic compensation). Plastic compensation is defined as adaptive plasticity overcoming maladaptive plasticity. In particular, plastic compensation may increase the likelihood of genetic compensation by facilitating population persistence. We provide key terms to disentangle these aspects of phenotypic plasticity and introduce examples to reinforce the potential importance of plastic compensation for understanding evolutionary change [Current Zoology 59 (4): 526–536, 2013].

Evolutionary stasis characterizes many phenotypes, even ones that seem suboptimal. Among tapeworms, Schistocephalus solidus and its relatives have some of the shortest developmental times in their first intermediate hosts, yet their development still seems excessively long considering they can grow faster, larger, and safer in the next hosts in their complex life cycles. I conducted 4 generations of selection on the developmental rate of S. solidus in its copepod first host, pushing a conserved-but-counterintuitive phenotype toward the limit of known tapeworm life-history strategies. Faster parasite development evolved and enabled earlier infectivity to the stickleback next host, but low heritability for infectivity moderated fitness gains. Fitness losses were more pronounced for slow-developing parasite families, irrespective of selection line, because directional selection released linked genetic variation for reduced infectivity to copepods, developmental stability, and fecundity. This deleterious variation is normally suppressed, implying development is canalized and thus under stabilizing selection. Nevertheless, faster development was not costly; fast-developing genotypes did not decrease copepod survival, even under host starvation, nor did they underperform in the next hosts, suggesting parasite stages in successive hosts are genetically decoupled. I speculate that, on longer time scales, the ultimate cost of abbreviated development is reduced size-dependent infectivity., (© The Author(s) 2023. Published by Oxford University Press on behalf of The Society for the Study of Evolution (SSE).)

Developmental robustness represents the ability of an organism to resist phenotypic variations despite environmental insults and inherent genetic variations. Derailment of developmental robustness leads to phenotypic variations that can get fixed in a population for many generations. Environmental pollution is a significant worldwide problem with detrimental consequences of human development. Understanding the genetic basis for how pollutants affect human development is critical for developing interventional therapies. Here, we report that environmental stress induced by hexavalent chromium, Cr(VI), a potent industrial pollutant, compromises developmental robustness, leading to phenotypic variations in the progeny. These phenotypic variations arise due to epigenetic instability and transposon activation in the somatic tissues of the progeny rather than novel genetic mutations and can be reduced by increasing the dosage of Piwi - a Piwi-interacting RNA-binding protein, in the ovary of the exposed mother. Significantly, the derailment of developmental robustness by Cr(VI) exposure leads to tumors in the progeny, and the predisposition to develop tumors is fixed in the population for at least three generations. Thus, we show for the first time that environmental pollution can derail developmental robustness and predispose the progeny of the exposed population to develop phenotypic variations and tumors., (© The Author(s) 2023. Published by Oxford University Press.)

Morphological analyses are critical to quantify phenotypic variation, identify taxa, inform phylogenetic relationships, and shed light on evolutionary patterns. This work is particularly important in groups that display great morphological disparity. Such is the case in geomyoid rodents, a group that includes 2 of the most species-rich families of rodents in North America: the Geomyidae (pocket gophers) and the Heteromyidae (kangaroo rats, pocket mice, and their relatives). We assessed variation in skull morphology (including both shape and size) among geomyoids to test the hypothesis that there are statistically significant differences in skull measurements at the family, genus, and species levels. Our sample includes 886 specimens representing all geomyoid genera and 39 species. We used the geometric mean to compare size across taxa. We used 14 measurements of the cranium and lower jaw normalized for size to compare shape among and within taxa. Our results show that skull measurements enable the distinction of geomyoids at the family, genus, and species levels. There is a larger amount of size variation within Geomyidae than within Heteromyidae. Our phylomorphospace analysis shows that the skull shape of the common ancestor of all geomyoids was more similar to the common ancestor of heteromyids than that of geomyids. Geomyid skulls display negative allometry whereas heteromyid skulls display positive allometry. Within heteromyids, dipodomyines, and non-dipodomyines show significantly different allometric patterns. Future analyses including fossils will be necessary to test our evolutionary hypotheses., Competing Interests: The authors declare no conflict of interest., (© The Author(s) 2022. Published by Oxford University Press on behalf of Editorial Office, Current Zoology.)

Early experience can prepare offspring to adapt their behaviors to the environment they are likely to encounter later in life. In several species of ants, colonies show ontogenic changes in the brood-to-worker ratio that are known to have an impact on worker morphology. However, little information is available on the influence of fluctuations in the early social context on the expression of behavior in adulthood. Using the ant Lasius niger , we tested whether the brood-to-worker ratio during larval stages influenced the level of behavioral variability at adult stages. We raised batches of 20 or 180 larvae in the presence of 60 workers until adulthood. We then quantified the activity level and wall-following tendency of callow workers on 10 successive trials to test the prediction that larvae reared under a high brood-to-worker ratio should show greater behavioral variations. We found that manipulation of the brood-to-worker ratio influenced the duration of development and the size of individuals at emergence. We detected no influence of early social context on the level of between- or within-individual variation measured for individual activity level or on wall-following behavior. Our study suggests that behavioral traits may be more canalized than morphological traits., (© The Author(s) (2021). Published by Oxford University Press on behalf of Editorial Office, Current Zoology.)

Mutations shape genetic architecture and thus influence the evolvability, adaptation and diversification of populations. Mutations may have different and even opposite effects on separate fitness components, and their rate of origin, distribution of effects and variance-covariance structure may depend on environmental quality. We performed an approximately 1,500-generation mutation-accumulation (MA) study in diploids of the yeast Saccharomyces cerevisiae in stressful (high-salt) and normal environments (50 lines each) to investigate the rate of input of mutational variation ( V ) as well as the mutation rate and distribution of effects on diploid and haploid fitness components, assayed in the normal environment. All four fitness components in both MA treatments exhibited statistically significant mutational variance and mutational heritability. Compared to normal-MA, salt stress increased the mutational variance in growth rate by more than sevenfold in haploids derived from the MA lines. This increase was not detected in diploid growth rate, suggesting masking of mutations in the heterozygous state. The genetic architecture arising from mutation (M-matrix) differed between normal and salt conditions. Salt stress also increased environmental variance in three fitness components, consistent with a reduction in canalization. Maximum-likelihood analysis indicated that stress increased the genomic mutation rate by approximately twofold for maximal growth rate and sporulation rate in diploids and for viability in haploids, and by tenfold for maximal growth rate in haploids, but large confidence intervals precluded distinguishing these values between MA environments. We discuss correlations between fitness components in diploids and haploids and compare the correlations between the two MA environmental treatments.m ) as well as the mutation rate and distribution of effects on diploid and haploid fitness components, assayed in the normal environment. All four fitness components in both MA treatments exhibited statistically significant mutational variance and mutational heritability. Compared to normal-MA, salt stress increased the mutational variance in growth rate by more than sevenfold in haploids derived from the MA lines. This increase was not detected in diploid growth rate, suggesting masking of mutations in the heterozygous state. The genetic architecture arising from mutation (M-matrix) differed between normal and salt conditions. Salt stress also increased environmental variance in three fitness components, consistent with a reduction in canalization. Maximum-likelihood analysis indicated that stress increased the genomic mutation rate by approximately twofold for maximal growth rate and sporulation rate in diploids and for viability in haploids, and by tenfold for maximal growth rate in haploids, but large confidence intervals precluded distinguishing these values between MA environments. We discuss correlations between fitness components in diploids and haploids and compare the correlations between the two MA environmental treatments., (Copyright © 2020 Kozela, Johnston.)

Organisms are exposed to environmental and mutational effects influencing both mean and variance of phenotypes. Potentially deleterious effects arising from this variation can be reduced by the evolution of buffering (canalizing) mechanisms, ultimately reducing phenotypic variability. There has been interest regarding the conditions enabling the evolution of canalization. Under some models, the circumstances under which genetic canalization evolves are limited despite apparent empirical evidence for it. It has been argued that genetic canalization evolves as a correlated response to environmental canalization (congruence model). Yet, empirical evidence has not consistently supported predictions of a correlation between genetic and environmental canalization. In a recent study, a population of Drosophila adapted to high altitude showed evidence of genetic decanalization relative to those from low altitudes. Using strains derived from these populations, we tested if they varied for multiple aspects of environmental canalization We observed the expected differences in wing size, shape, cell (trichome) density and mutational defects between high- and low-altitude populations. However, we observed little evidence for a relationship between measures of environmental canalization with population or with defect frequency. Our results do not support the predicted association between genetic and environmental canalization., (© 2020 The Authors. Evolution © 2020 The Society for the Study of Evolution.)

Phenotypic plasticity is defined as the property of organisms to produce distinct phenotypes in response to environmental variation. While for more than a century, biologists have proposed this organismal feature to play an important role in evolution and the origin of novelty, the idea has remained contentious. Plasticity is found in all domains of life, but only recently has there been an increase in empirical studies. This contribution is intended as a fresh view and will discuss current and future challenges of plasticity research, and the need to identify associated molecular mechanisms. After a brief summary of conceptual, theoretical, and historical aspects, some of which were responsible for confusion and contention, I will formulate three major research directions and predictions for the role of plasticity as a facilitator of novelty. These predictions result in a four-step model that, when properly filled with molecular mechanisms, will reveal plasticity as a major factor of evolution. Such mechanistic insight must be complemented with comparative investigations to show that plasticity has indeed created novelty and innovation. Together, such studies will help develop a true developmental evolutionary biology., (Copyright © 2020 by the Genetics Society of America.)

Background and Aims: Phenotypic plasticity and genetic differentiation both play important roles in the establishment and spread of species after extra-range dispersal; however, the adaptive potential of plasticity and genetic divergence in successful invasions remains unclear., Methods: We measured six anatomical traits associated with drought tolerance in contrasting water environments for individuals from the invasive and native range of the bunchgrass Brachypodium sylvaticum. To represent sources contributing to admixed genotypes in the invasive range accurately, we used unique alleles to determine probabilities of genetic contribution, and utilized these as weights in our analyses. The adaptive values of plasticity and genetic differentiation were assessed using regression., Key Results: No plasticity was found in response to water availability for any of the measured traits. Bulliform cell area and three traits related to xylem morphology displayed genetic differentiation between invasive and native ranges, indicating a shift in the invasive range towards drought-tolerant phenotypes. Genetic divergence was not consistently in the direction indicated by selection, suggesting that responses are limited by trade-offs with other traits or physical constraints., Conclusions: Our results indicate that invasive adaptation is the consequence of post-introduction selection leading to genetic differentiation. Selection, rather than plasticity, is driving B. sylvaticum success in its invaded range., (© The Author(s) 2018. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)

Background: The presence of a polar auxin transport stream has long been correlated with the differentiation and patterning of vascular cells across vascular plants. As our understanding of auxin transport and vascular development has grown, so too has evidence for the correlation between these processes. However, a clear understanding of the cellular and molecular mechanisms driving this correlation has not been elucidated., Scope: This article examines the hypothesis that canalization via polar auxin transport regulates vascular reconnection and patterning in the stem after wounding or grafting. We examine the evidence for the causal nature of the relationship and the suggested role that other hormones may play. Data are presented indicating that in grafted plants the degree of auxin transport may not always correlate with vascular reconnection. Furthermore, data on grafting success using plants with a range of hormone-related mutations indicate that these hormones may not be critical for vascular reconnection., Conclusions: In the past, excellent work examining elements of auxin synthesis, transport and response in relation to vascular development has been carried out. However, new experimental approaches are required to test more directly the hypothesis that auxin transport regulates stem vascular reconnection after wounding or grafting. This could include studies on the timing of the re-establishment of auxin transport and vascular reconnection after grafting and the influence of auxin transport mutants and inhibitors on these processes using live imaging., (© The Author(s) 2018. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)

Genome-wide heterozygosity has long been hypothesized to play a role in buffering organisms against developmental perturbations, potentially resulting in increased symmetry. If true, this could in part explain the maintenance of standing genetic variation in wild populations. Marine threespine sticklebacks (Gasterosteus aculeatus) were sampled across their eastern Pacific coastal distribution from Alaska to California and variations in asymmetry for both structural and nonstructural armor traits (lateral plates) were assessed. Structural plates consistently showed less asymmetry than nonstructural plates, but standardized measures of heterozygosity were not correlated with the extent of asymmetry expressed by a fish. Fish that were heterozygous for the major-effect gene controlling lateral plate variation (Ectodysplasin) had higher occurrences of asymmetry, even when the individuals were phenotypically fully plated. Collectively, this suggests that heterozygosity at a major-effect locus can have a greater impact on asymmetry than heterozygosity sampled across the genome., (© 2018 The Author(s). Evolution © 2018 The Society for the Study of Evolution.)

Natural selection may enhance or weaken the robustness of phenotypes against genetic or environmental perturbations. However, important aspects of the relationship between adaptive evolution and canalization remain unclear. Recent work showed that the evolution of larger wing size in a high altitude natural population of Drosophila melanogaster was accompanied by decanalized wing development--specifically a loss of robustness to genetic perturbation. But this study did not address environmental robustness, and it compared populations that may have numerous biological differences. Here, we perform artificial selection on this same trait in D. melanogaster (larger wing length) and directly test whether this directional selection resulted in decanalization. We find that in general, size-selected replicates show greater frequencies of wing defects than control replicates both after mutagenesis (genetic perturbation) and when subjected to high temperature stress (environmental perturbation), although the increase in defect frequency varies importantly among replicates. These results support the hypothesis that directional selection may result in the loss of both genetic and environmental robustness-offering a rare window into the relationship between adaptation and canalization., (© 2018 The Author(s). Evolution © 2018 The Society for the Study of Evolution.)

Background and Aims: Many plant-pollinator interactions are mediated by floral scents that can vary among species, among populations within species and even among individuals within populations. This variation could be innate and unaffected by the environment, but, because many floral volatiles have amino-acid precursors, scent variation also could be affected by differences in nutrient availability among environments. In plants that have coevolved with specific pollinators, natural selection is likely to favour low phenotypic plasticity in floral scent even under different conditions of nutrient availability if particular scents or scent combinations are important for attracting local pollinators., Methods: Clonal pairs of multiple seed-families of two Lithophragma bolanderi (Saxifragaceae) populations were subjected to a high and a low nutrient treatment. These plants are pollinated primarily by host-specific Greya moths. It was evaluated how nutrient treatment affected variation in floral scent relative to other vegetative and reproductive traits., Key Results: Floral scent strength (the per-flower emission rate) and composition were unaffected by nutrient treatment, but low-nutrient plants produced fewer and lighter leaves, fewer scapes and fewer flowers than high-nutrient plants. The results held in both populations, which differed greatly in the number and composition of floral scents produced., Conclusions: The results reveal a strong genetic component both to scent composition and emission level, and partly contrasts with the only previous study that has assessed the susceptibility of floral volatile signals to variation in the abundance of nutrients. These results, and the tight coevolutionary relationship between Lithophragma plants and their specialized Greya moth pollinators, indicate that reproductive traits important to coevolving interactions, such as the floral scent of L. bolanderi, may be locally specialized and more canalized than other traits important for plant fitness., (© The Author 2017. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: journals.permissions@oup.com)

One of the most fascinating scientific problems, and a subject of intense debate, is that of the mechanisms of biological evolution. In this context, Waddington elaborated the concepts of "canalization and assimilation" to explain how an apparently somatic variant induced by stress could become heritable through the germline in Drosophila He resolved this seemingly Lamarckian phenomenon by positing the existence of cryptic mutations that can be expressed and selected under stress. To investigate the relevance of such mechanisms, we performed experiments following the Waddington procedure, then isolated and fixed three phenotypic variants along with another induced mutation that was not preceded by any phenocopy. All the fixed mutations we looked at were actually generated de novo by DNA deletions or transposon insertions, highlighting a novel mechanism for the assimilation process. Our study shows that heat-shock stress produces both phenotypic variants and germline mutations, and suggests an alternative explanation to that of Waddington for the apparent assimilation of an acquired character. The selection of the variants, under stress, for a number of generations allows for the coselection of newly induced corresponding germline mutations, making the phenotypic variants appear heritable., (Copyright © 2017 by the Genetics Society of America.)

The genetic basis of stochastic variation within a defined environment, and the consequences of such micro-environmental variance for fitness are poorly understood . Using a multigenerational breeding design in Drosophila serrata , we demonstrated that the micro-environmental variance in a set of morphological wing traits in a randomly mating population had significant additive genetic variance in most single wing traits. Although heritability was generally low (<1%), coefficients of additive genetic variance were of a magnitude typical of other morphological traits, indicating that the micro-environmental variance is an evolvable trait. Multivariate analyses demonstrated that the micro-environmental variance in wings was genetically correlated among single traits, indicating that common mechanisms of environmental buffering exist for this functionally related set of traits. In addition, through the dominance genetic covariance between the major axes of micro-environmental variance and fitness, we demonstrated that micro-environmental variance shares a genetic basis with fitness, and that the pattern of selection is suggestive of variance-reducing selection acting on micro-environmental variance., (Copyright © 2017 by the Genetics Society of America.)

Phenotypic plasticity is increasingly recognized to facilitate adaptive change in plants and animals, including insects, nematodes, and vertebrates. Plasticity can occur as continuous or discrete (polyphenisms) variation. In social insects, for example, in ants, some species have workers of distinct size classes while in other closely related species variation in size may be continuous. Despite the abundance of examples in nature, how discrete morphs are specified remains currently unknown. In theory, polyphenisms might require robustness, whereby the distribution of morphologies would be limited by the same mechanisms that execute buffering from stochastic perturbations, a function attributed to heat-shock proteins of the Hsp90 family. However, this possibility has never been directly tested because plasticity and robustness are considered to represent opposite evolutionary principles. Here, we used a polyphenism of feeding structures in the nematode Pristionchus pacificus to test the relationship between robustness and plasticity using geometric morphometrics of 20 mouth-form landmarks. We show that reducing heat-shock protein activity, which reduces developmental robustness, increases the range of mouth-form morphologies. Specifically, elevated temperature led to a shift within morphospace, pharmacological inhibition of all Hsp90 genes using radicicol treatment increased shape variability in both mouth-forms, and CRISPR/Cas9-induced Ppa-daf-21/Hsp90 knockout had a combined effect. Thus, Hsp90 canalizes the morphologies of plastic traits resulting in discrete polyphenism of mouth-forms., (© The Author 2017. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.)

The structure of environmentally induced phenotypic covariation can influence the effective strength and magnitude of natural selection. Yet our understanding of the factors that contribute to and influence the evolutionary lability of such covariation is poor. Most studies have either examined environmental variation without accounting for covariation, or examined phenotypic and genetic covariation without distinguishing the environmental component. In this study, we examined the effect of mutational perturbations on different properties of environmental covariation, as well as mean shape. We use strains of Drosophila melanogaster bearing well-characterized mutations known to influence wing shape, as well as naturally derived strains, all reared under carefully controlled conditions and with the same genetic background. We find that mean shape changes more freely than the covariance structure, and that different properties of the covariance matrix change independently from each other. The perturbations affect matrix orientation more than they affect matrix eccentricity or total variance. Yet, mutational effects on matrix orientation do not cluster according to the developmental pathway that they target. These results suggest that it might be useful to consider a more general concept of "decanalization," involving all aspects of variation and covariation., (© 2016 The Author(s). Evolution © 2016 The Society for the Study of Evolution.)

Background: Discussions of phenotypic robustness often consider scenarios where invariant phenotypes are optimal and assume that developmental mechanisms have evolved to buffer the phenotypes of specific traits against stochastic and environmental perturbations. However, plastic plant phenotypes that vary between environments or variable phenotypes that vary stochastically within an environment may also be advantageous in some scenarios., Scope: Here the conditions under which invariant, plastic and variable phenotypes of specific traits may confer a selective advantage in plants are examined. Drawing on work from microbes and multicellular organisms, the mechanisms that may give rise to each type of phenotype are discussed., Conclusion: In contrast to the view of robustness as being the ability of a genotype to produce a single, invariant phenotype, changes in a phenotype in response to the environment, or phenotypic variability within an environment, may also be delivered consistently (i.e. robustly). Thus, for some plant traits, mechanisms have probably evolved to produce plasticity or variability in a reliable manner., (© The Author 2016. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: journals.permissions@oup.com.)

Background: Most, if not all, organisms possess the ability to alter their phenotype in direct response to changes in their environment, a phenomenon known as phenotypic plasticity. Selection can break this environmental sensitivity, however, and cause a formerly environmentally induced trait to evolve to become fixed through a process called genetic assimilation. Essentially, genetic assimilation can be viewed as the evolution of environmental robustness in what was formerly an environmentally sensitive trait. Because genetic assimilation has long been suggested to play a key role in the origins of phenotypic novelty and possibly even new species, identifying and characterizing the proximate mechanisms that underlie genetic assimilation may advance our basic understanding of how novel traits and species evolve., Scope: This review begins by discussing how the evolution of phenotypic plasticity, followed by genetic assimilation, might promote the origins of new traits and possibly fuel speciation and adaptive radiation. The evidence implicating genetic assimilation in evolutionary innovation and diversification is then briefly considered. Next, the potential causes of phenotypic plasticity generally and genetic assimilation specifically are examined at the genetic, molecular and physiological levels and approaches that can improve our understanding of these mechanisms are described. The review concludes by outlining major challenges for future work., Conclusions: Identifying and characterizing the proximate mechanisms involved in phenotypic plasticity and genetic assimilation promises to help advance our basic understanding of evolutionary innovation and diversification., (© The Author 2015. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: journals.permissions@oup.com.)

Background: Living organisms are continuously confronted with perturbations, such as environmental changes that include fluctuations in temperature and nutrient availability, or genetic changes such as mutations. While some developmental systems are affected by such challenges and display variation in phenotypic traits, others continue consistently to produce invariable phenotypes despite perturbation. This ability of a living system to maintain an invariable phenotype in the face of perturbations is termed developmental robustness. Biological robustness is a phenomenon observed across phyla, and studying its mechanisms is central to deciphering the genotype-phenotype relationship. Recent work in yeast, animals and plants has shown that robustness is genetically controlled and has started to reveal the underlying mechinisms behind it., Scope and Conclusions: Studying biological robustness involves focusing on an important property of developmental traits, which is the phenotypic distribution within a population. This is often neglected because the vast majority of developmental biology studies instead focus on population aggregates, such as trait averages. By drawing on findings in animals and yeast, this Viewpoint considers how studies on plant developmental robustness may benefit from strict definitions of what is the developmental system of choice and what is the relevant perturbation, and also from clear distinctions between gene effects on the trait mean and the trait variance. Recent advances in quantitative developmental biology and high-throughput phenotyping now allow the design of targeted genetic screens to identify genes that amplify or restrict developmental trait variance and to study how variation propagates across different phenotypic levels in biological systems. The molecular characterization of more quantitative trait loci affecting trait variance will provide further insights into the evolution of genes modulating developmental robustness. The study of robustness mechanisms in closely related species will address whether mechanisms of robustness are evolutionarily conserved., (© The Author 2015. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: journals.permissions@oup.com.)

Background and Aims: Brassicaceae is one of the most diversified families in the angiosperms. However, most species from this family exhibit a very similar floral bauplan. In this study, we explore the Brassicaceae floral morphospace, examining how corolla shape variation (an estimation of developmental robustness), integration and disparity vary among phylogenetically related species. Our aim is to check whether these floral attributes have evolved in this family despite its apparent morphological conservation, and to test the role of pollinators in driving this evolution., Methods: Using geometric morphometric tools, we calculated the phenotypic variation, disparity and integration of the corolla shape of 111 Brassicaceae taxa. We subsequently inferred the phylogenetic relationships of these taxa and explored the evolutionary lability of corolla shape. Finally, we sampled the pollinator assemblages of every taxon included in this study, and determined their pollination niches using a modularity algorithm. We explore the relationship between pollination niche and the attributes of corolla shape., Key Results: Phylogenetic signal was weak for all corolla shape attributes. All taxa had generalized pollination systems. Nevertheless, they belong to different pollination niches. There were significant differences in corolla shape among pollination niches even after controlling for the phylogenetic relationship of the plant taxa. Corolla shape variation and disparity was significantly higher in those taxa visited mostly by nocturnal moths, indicating that this pollination niche is associated with a lack of developmental robustness. Corolla integration was higher in those taxa visited mostly by hovering long-tongued flies and long-tongued large bees., Conclusions: Corolla variation, integration and disparity were evolutionarily labile and evolved very recently in the evolutionary history of the Brassicaceae. These floral attributes were strongly related to the pollination niche. Even in a plant clade having a very generalized pollination system and exhibiting a conserved floral bauplan, pollinators can drive the evolution of important developmental attributes of corolla shape., (© The Author 2016. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: journals.permissions@oup.com.)

Background: Robustness to genetic and environmental perturbation is a salient feature of multicellular organisms. Loss of developmental robustness can lead to severe phenotypic defects and fitness loss. However, perfect robustness, i.e. no variation at all, is evolutionarily unfit as organisms must be able to change phenotype to properly respond to changing environments and biotic challenges. Plasticity is the ability to adjust phenotypes predictably in response to specific environmental stimuli, which can be considered a transient shift allowing an organism to move from one robust phenotypic state to another. Plants, as sessile organisms that undergo continuous development, are particularly dependent on an exquisite fine-tuning of the processes that balance robustness and plasticity to maximize fitness., Scope and Conclusions: This paper reviews recently identified mechanisms, both systems-level and molecular, that modulate robustness, and discusses their implications for the optimization of plant fitness. Robustness in living systems arises from the structure of genetic networks, the specific molecular functions of the underlying genes, and their interactions. This very same network responsible for the robustness of specific developmental states also has to be built such that it enables plastic yet robust shifts in response to environmental changes. In plants, the interactions and functions of signal transduction pathways activated by phytohormones and the tendency for plants to tolerate whole-genome duplications, tandem gene duplication and hybridization are emerging as major regulators of robustness in development. Despite their obvious implications for plant evolution and plant breeding, the mechanistic underpinnings by which plants modulate precise levels of robustness, plasticity and evolvability in networks controlling different phenotypes are under-studied., (© The Author 2015. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: journals.permissions@oup.com.)

Genetic and environmental factors influence complex disease in humans, such as metabolic syndrome, and Drosophila melanogaster serves as an excellent model in which to test these factors experimentally. Here we explore the modularity of endophenotypes with an in-depth reanalysis of a previous study by Reed et al. (2014), where we raised 20 wild-type genetic lines of Drosophila larvae on four diets and measured gross phenotypes of body weight, total sugar, and total triglycerides, as well as the endophenotypes of metabolomic and whole-genome expression profiles. We then perform new gene expression experiments to test for conservation of phenotype-expression correlations across different diets and populations. We find that transcript levels correlated with gross phenotypes were enriched for puparial adhesion, metamorphosis, and central energy metabolism functions. The specific metabolites L-DOPA and N-arachidonoyl dopamine make physiological links between the gross phenotypes across diets, whereas leucine and isoleucine thus exhibit genotype-by-diet interactions. Between diets, we find low conservation of the endophenotypes that correlate with the gross phenotypes. Through the follow-up expression study, we found that transcript-trait correlations are well conserved across populations raised on a familiar diet, but on a novel diet, the transcript-trait correlations are no longer conserved. Thus, physiological canalization of metabolic phenotypes breaks down in a novel environment exposing cryptic variation. We cannot predict the physiological basis of disease in a perturbing environment from profiles observed in the ancestral environment. This study demonstrates that variation for disease traits within a population is acquired through a multitude of physiological mechanisms, some of which transcend genetic and environmental influences, and others that are specific to an individual's genetic and environmental context., (Copyright © 2015 Williams et al.)

The Mediterranean region is an area of special interest for conservation where the incidence of multiple drivers of global change is expected to increase. One of the factors predicted to change is soil-nutrient availability, an essential factor for plant growth. Thus, study of the effects of variation in this parameter is especially relevant in species with a circum-Mediterranean distribution, such as Arbutus unedo L., in which the different provenances grow in different habitats, which must differ in nutritional conditions. We aimed to determine the effect of provenance on plasticity, to establish whether structural and morphological traits differ in the level of plasticity and to assess how nutrients affect the photosynthetic light response. In a common garden experiment, we studied seven provenances from the circum-Mediterranean range of A. unedo and established two nutrient treatments (low and high nutrient availability). We measured physiological and structural traits in 1-year-old sapling and determined a phenotypic plasticity index (PPI) to quantify the level of plasticity, whereas the radiation effects were tested by construction and analysis of light response curves. Interestingly, provenance did not explain a significant amount of variance, but the plasticity was four times higher for the structural traits than for the physiological traits. Therefore, the plasticity to nutrient availability will not favour or prevent the expansion or contraction of the range of any of these provenances of A. unedo. Furthermore, the structural plasticity demonstrated the ability of the strawberry tree to optimize resource allocation, whereas the physiology remained stable, thus avoiding extra expenditure. The study findings also suggest that increased availability of nutrients would improve the performance of the species during the Mediterranean summer, characterized by high irradiance. These abilities will be key to the survival of saplings of the species under the future scenario of changes in nutrient availability., (© The Author 2015. Published by Oxford University Press. All rights reserved. For Permissions, please email: journals.permissions@oup.com.)

The plant hormone auxin plays an essential role in the patterning of plant structures. Biological hypotheses supported by computational models suggest that auxin may fulfil this role by regulating its own transport, but the plausibility of previously proposed models has been questioned. We applied the notion of unidirectional fluxes and the formalism of Petri nets to show that the key modes of auxin-driven patterning-the formation of convergence points and the formation of canals-can be implemented by biochemically plausible networks, with the fluxes measured by dedicated tally molecules or by efflux and influx carriers themselves. Common elements of these networks include a positive feedback of auxin efflux on the allocation of membrane-bound auxin efflux carriers (PIN proteins), and a modulation of this allocation by auxin in the extracellular space. Auxin concentration in the extracellular space is the only information exchanged by the cells. Canalization patterns are produced when auxin efflux and influx act antagonistically: an increase in auxin influx or concentration in the extracellular space decreases the abundance of efflux carriers in the adjacent segment of the membrane. In contrast, convergence points emerge in networks in which auxin efflux and influx act synergistically. A change in a single reaction rate may result in a dynamic switch between these modes, suggesting plausible molecular implementations of coordinated patterning of organ initials and vascular strands predicted by the dual polarization theory., (© The Author 2015. Published by Oxford University Press on behalf of the Society for Experimental Biology.)

Many organisms survive fluctuating and extreme environmental conditions by manifesting multiple distinct phenotypes during adulthood by means of developmental processes that enable phenotypic plasticity. We report on the discovery of putative plasticity-enabling genes that are involved in transforming the gill of the euryhaline teleost fish, Fundulus heteroclitus, from its freshwater to its seawater gill-type, a process that alters both morphology and function. Gene expression that normally enables osmotic plasticity is inhibited by arsenic. Gene sets defined by antagonistic interactions between arsenic and salinity show reduced transcriptional variation among individual fish, suggesting unusually accurate and precise regulatory control of these genes, consistent with the hypothesis that they participate in a canalized developmental response. We observe that natural selection acts to preserve canalized gene expression in populations of killifish that are most tolerant to abrupt salinity change and that these populations show the least variability in their transcription of genes enabling plasticity of the gill. We found that genes participating in this highly canalized and conserved plasticity-enabling response had significantly fewer and less complex associations with transcriptional regulators than genes that respond only to arsenic or salinity. Collectively these findings, which are drawn from the relationships between environmental challenge, plasticity, and canalization among populations, suggest that the selective processes that facilitate phenotypic plasticity do so by targeting the regulatory networks that gives rise to the response. These findings also provide a generalized, conceptual framework of how genes might interact with the environment and evolve toward the development of plastic traits., (© The Author 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.)

Most phenotypic traits are controlled by many genes, but a global picture of the genotype-phenotype map (GPM) is lacking. For example, in no species do we know generally how many genes affect a trait and how large these effects are. It is also unclear to what extent GPMs are shaped by natural selection. Here we address these fundamental questions using the reverse genetic data of 220 morphological traits in 4,718 budding yeast strains, each of which lacks a nonessential gene. We show that 1) the proportion of genes affecting a trait varies from <1% to >30%, averaging 6%, 2) most traits are impacted by many more small-effect genes than large-effect genes, and 3) the mean effect of all nonessential genes on a trait decreases precipitously as the estimated importance of the trait to fitness increases. An analysis of 3,116 yeast gene expression traits in 754 gene-deletion strains reveals a similar pattern. These findings illustrate the power of genome-wide reverse genetics in genotype-phenotype mapping, uncover an enormous range of genetic complexity of phenotypic traits, and suggest that the GPM of cellular organisms has been shaped by natural selection for mutational robustness., (© The Author 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)

Genetic potential for evolutionary change and covariational constraints are typically summarized as the genetic variance-covariance matrix G, and there is currently debate over the extent to which G remains effectively constant during the course of adaptive evolution. However, G provides only a temporally restricted view of constraints that ignores possible biases in how new mutations affect multivariate phenotypes. We used chemical mutagenesis to study the effect of mutations as summarized by the mutational covariance matrix, M, in Arabidopsis thaliana. By introducing mutations into three isogenic strains of A. thaliana, we were able to quantify M directly as the genetic variance-covariance matrix of mutagenized lines. Induced mutations generally did not alter the means of the six morphology and life-history traits we measured, but they did affect the levels of available genetic variation and the covariances among traits. However, these effects were not consistent among the three isogenic lines; that is, there were significant differences among the lines in both the number of mutations produced by ethyl-methane-sulfonate treatment and the M matrices they induced. The evolutionary implications of the dependence of M on the number of mutations, the particular genetic background, and the mutagenic sampling of loci in the genome are discussed in light of commonly applied models of multivariate evolution and the potential for the genetic architecture itself to change in ways that facilitate the coordinated evolution of complex phenotypes., (© 1999 The Society for the Study of Evolution.)

Evolution can change the developmental processes underlying a character without changing the average expression of the character itself. This sort of change must occur in both the evolution of canalization, in which a character becomes increasingly buffered against genetic or developmental variation, and in the phenomenon of closely related species that show similar adult phenotypes but different underlying developmental patterns. To study such phenomena, I develop a model that follows evolution on a surface representing adult phenotype as a function of underlying developmental characters. A contour on such a "phenotype landscape" is a set of states of developmental characters that produce the same adult phenotype. Epistasis induces curvature of this surface, and degree of canalization is represented by the slope along a contour. I first discuss the geometric properties of phenotype landscapes, relating epistasis to canalization. I then impose a fitness function on the phenotype and model evolution of developmental characters as a function of the fitness function and the local geometry of the surface. This model shows how canalization evolves as a population approaches an optimum phenotype. It further shows that under some circumstances, "decanalization" can occur, in which the expression of adult phenotype becomes increasingly sensitive to developmental variation. This process can cause very similar populations to diverge from one another developmentally even when their adult phenotypes experience identical selection regimes., (© 1998 The Society for the Study of Evolution.)

Canalization is the suppression of phenotypic variation. Depending on the causes of phenotypic variation, one speaks either of genetic or environmental canalization. Genetic canalization describes insensitivity of a character to mutations, and the insensitivity to environmental factors is called environmental canalization. Genetic canalization is of interest because it influences the availability of heritable phenotypic variation to natural selection, and is thus potentially important in determining the pattern of phenotypic evolution. In this paper a number of population genetic models are considered of a quantitative character under stabilizing selection. The main purpose of this study is to define the population genetic conditions and constraints for the evolution of canalization. Environmental canalization is modeled as genotype specific environmental variance. It is shown that stabilizing selection favors genes that decrease environmental variance of quantitative characters. However, the theoretical limit of zero environmental variance has never been observed. Of the many ways to explain this fact, two are addressed by our model. It is shown that a "canalization limit" is reached if canalizing effects of mutations are correlated with direct effects on the same character. This canalization limit is predicted to be independent of the strength of stabilizing selection, which is inconsistent with recent experimental data (Sterns et al. 1995). The second model assumes that the canalizing genes have deleterious pleiotropic effects. If these deleterious effects are of the same magnitude as all the other mutations affecting fitness very strong stabilizing selection is required to allow the evolution of environmental canalization. Genetic canalization is modeled as an influence on the average effect of mutations at a locus of other genes. It is found that the selection for genetic canalization critically depends on the amount of genetic variation present in the population. The more genetic variation, the stronger the selection for canalizing effects. All factors that increase genetic variation favor the evolution of genetic canalization (large population size, high mutation rate, large number of genes). If genetic variation is maintained by mutation-selection balance, strong stabilizing selection can inhibit the evolution of genetic canalization. Strong stabilizing selection eliminates genetic variation to a level where selection for canalization does not work anymore. It is predicted that the most important characters (in terms of fitness) are not necessarily the most canalized ones, if they are under very strong stabilizing selection (k > 0.2V e ). The rate of decrease of mutational variance V m is found to be less than 10% of the initial V m . From this result it is concluded that characters with typical mutational variances of about 10 -3 V e are in a metastable state where further evolution of genetic canalization is too slow to be of importance at a microevolutionary time scale. The implications for the explanation of macroevolutionary patterns are discussed., (© 1997 The Society for the Study of Evolution.)

The effects of inbreeding on the phenotypic variance within populations were measured in a set of 30 bottlenecked lines derived from a single source population of Drosophila melanogaster. Inbred lines had significant variance among lines in the amount of phenotypic variance within lines, for thorax length, and sternopleural bristle scores. When significance levels were corrected on an experimentwide basis, no line had significant increases in phenotypic variance for sternopleural bristle counts, although two lines had significant increases in thorax length variance. These results demonstrate that inbred lines cannot be treated as necessarily more uniform than outbred lines and that results on changes in variance due to inbreeding should be treated with caution unless there has been sufficient replication. These results also demonstrate the validity of an important assumption of models of evolution by variance-mediated mechanisms, such as the variance-induced peak-shift model., (© 1996 The Society for the Study of Evolution.)

To investigate the consequences of canalization and plasticity in arthropod developmental pathways, we developed a model that predicts eight possible combinations among three larval developmental parameters. From the descriptions of insect and spider postembryonic development, it is apparent that not all aspects of juvenile development are plastic and that species differ in which traits are plastic. Most strikingly, only four of the possible eight combinations of canalized and plastic parameters have been found in nature. Using this model, we show that the identity of the canalized developmental parameters and the degree of genetic variation in the value at which a given parameter is fixed have important implications for the ecology and evolution of complex life cycles., (© 1996 The Society for the Study of Evolution.)

Canalization is an abstract term that describes unknown developmental mechanisms that reduce phenotypic variation. A trait can be canalized against environmental perturbations (e.g., changes in temperature or nutrient quality), or genetic perturbations (e.g., mutations or recombination); this paper is about genetic canalization. Stabilizing selection should improve the canalization of traits, and the degree of canalization should be positively correlated with the traits' impact on fitness. Experiments testing this idea should measure the canalization of a series of traits whose impact on fitness is known or can be inferred, exclude differences among traits in the number of loci and alleles segregating as an explanation for the pattern of variability found, and distinguish between canalization against genetic and environmental variation. These conditions were met by three experiments within which the variation of fitness components among Drosophila melanogaster lines was measured and among which the genetic contribution to the variation among lines was clearly different. The canalization of the traits increased with their impact on fitness and did not depend on the degree of genetic differences among lines. That the flies used had been transformed by a P-element insert suggests that canalization was also effective against novel genetic variation. The results reported here cannot be explained by the classical hypothesis of reduction in the number of loci segregating for traits with greater impact on fitness and confirm that traits with greater impact on fitness are more strongly canalized. This pattern of canalization reveals an underappreciated role for development in microevolution. There is differential genetic canalization of fitness components in D. melanogaster., (© 1994 The Society for the Study of Evolution.)