Consequences of inter-population crosses on developmental stability and canalization of floral traits in Dalechampia scandens (Euphorbiaceae)

Congruence between changes in phenotypic variance and developmental noise in inter-population hybrids was analysed to test whether environmental canalization and developmental stability were controlled by common genetic mechanisms. Developmental stability assessed by the level of fluctuating asymmetry (FA), and canalization by the within- and among-individual variance, were measured on several floral traits of Dalechampia scandens (Euphorbiaceae). Hybridization affected canalization. Both within- and among-individual phenotypic variance decreased in hybrids from populations of intermediate genetic distance, and strongly increased in hybrids from genetically distant populations. Mean-trait FA differed among cross-types, but hybrids were not consistently more or less asymmetric than parental lines across traits. We found no congruence between changes in FA and changes in phenotypic variance. These results suggest that developmental stability (measured by FA) and canalization are independently controlled. This study also confirms the weak relationship between FA and the breakdown of coadapted gene complexes following inter-population hybridization.     

No relationship between canalization and developmental stability of the skull in a natural population of Mastomys natalensis (Rodentia: Muridae)

The aim of the present work was to investigate the relationship between canalization and developmental stability under varying environmental conditions. Three different cohorts of Mastomys natalensis (Rodentia, Muridae), displaying different growth trajectories, were analysed by means of geometric morphometrics. A set of 23 landmarks was digitalized on the dorsal skull of 292 specimens from Morogoro (Tanzania). Patterns of among‐ and within‐individual (measured as fluctuating asymmetry, FA) variation were assessed and compared among and within the three groups to test for the presence of a common mechanism between canalization and developmental stability. Results showed that there was no congruence between canalization and developmental stability: (1) levels of FA and among‐individual variation varied in a discordant fashion, (2) no correspondence between the variance–covariance matrix of among‐ and within individual variation was found, and (3) environmental effects were able to alter the covariance structure of among‐individual variation leaving patterns associated with fluctuating asymmetry unaffected. These findings support the view of multiple mechanisms underlying developmental buffering of shape variation. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 207–216.     

Variational and genetic properties of developmental stability in Dalechampia scandens

Because low developmental stability may compromise the precision with which adaptations can be reached, the variability and genetic basis of developmental stability are important evolutionary parameters. Developmental stability is also an important clue to understanding how traits are regulated to achieve their phenotypic target value. However, developmental stability must be studied indirectly through proxy variables, such as fluctuating asymmetry, that are suggested to have noisy and often nonlinear relationships to the underlying variable of interest. In this paper we first show that mean-standardized measures of variance and covariance in fluctuating asymmetry, unlike heritabilities, repeatabilities, and correlations, are linearly related to corresponding measures of variation in underlying developmental stability. We then examine the variational properties of developmental stability in a population of the Neotropical vine, Dalechampia scandens (Euphorbiaceae). By studying fluctuating asymmetry in a large number of floral characters in both selfed and outcrossed individuals in a diallel design, we assemble strong evidence that both additive genetic and individual variation and covariation in developmental stability are virtually absent in this population.     

Genetic structure of phenotypic robustness in the collaborative cross mouse diallel panel

Developmental stability and canalization describe the ability of developmental systems to minimize phenotypic variation in the face of stochastic micro‐environmental effects, genetic variation and environmental influences. Canalization is the ability to minimize the effects of genetic or environmental effects, whereas developmental stability is the ability to minimize the effects of micro‐environmental effects within individuals. Despite much attention, the mechanisms that underlie these two components of phenotypic robustness remain unknown. We investigated the genetic structure of phenotypic robustness in the collaborative cross (CC) mouse reference population. We analysed the magnitude of fluctuating asymmetry (FA) and among‐individual variation of cranial shape in reciprocal crosses among the eight parental strains, using geometric morphometrics and a diallel analysis based on a Bayesian approach. Significant differences among genotypes were found for both measures, although they were poorly correlated at the level of individuals. An overall positive effect of inbreeding was found for both components of variation. The strain CAST/EiJ exerted a positive additive effect on FA and, to a lesser extent, among‐individual variance. Sex‐ and other strain‐specific effects were not significant. Neither FA nor among‐individual variation was associated with phenotypic extremeness. Our results support the existence of genetic variation for both developmental stability and canalization. This finding is important because robustness is a key feature of developmental systems. Our finding that robustness is not related to phenotypic extremeness is consistent with theoretical work that suggests that its relationship to stabilizing selection is not straightforward.     

Postnatal Dynamics of Developmental Stability and Canalization of Lizard Head Shape Under Different Environmental Conditions

Developmental stability (DS) and canalization are key determinants of phenotypic variation. To provide a better understanding of how postnatal growth is involved in determining the effects of DS and canalization on phenotypic variation, we studied within- and among-individual variation in head shape in ontogenetic series of lizards inhabiting urban and rural environments. Urban lizards exhibited increased fluctuating asymmetry during the early postnatal stages, but asymmetry levels decreased during growth. By contrast, asymmetry remained constant across the investigated size range in the rural population. In addition, urban juveniles were more variable for symmetric shape and deviated more from the group shape-size allometric trajectory, but both indices declined across ontogeny. Congruent patterns of within- and among-individual variation suggest that both DS and canalization may rely on similar underlying mechanisms. Further, the ontogenetic reduction of variation in the urban population suggests that compensatory growth may aid in buffering phenotypic variation and correcting deviances from the established developmental path. Alternatively, passive mechanisms and population dynamics may also explain the decrease of phenodeviants in urban populations. Significant correlations between symmetric and asymmetric shape, as well as similar integration patterns between the two populations, suggest that similar developmental mechanisms regulate head shape in both environments. Overall, these results highlight the relevance of both pre- and post-natal dynamics in determining levels of phenotypic variation, enhancing our understanding of how organisms respond to perturbations to DS and canalization under stressful conditions.     

Associations between leaf developmental stability,variability, canalization,and phenotypic plasticity in Abutilon theophrasti

Developmental stability, canalization, and phenotypic plasticity are the most common sources of phenotypic variation, yet comparative studies investigating the relationships between these sources, specifically in plants, are lacking. To investigate the relationships among developmental stability or instability, developmental variability, canalization, and plasticity in plants, we conducted a field experiment with Abutilon theophrasti, by subjecting plants to three densities under infertile vs. fertile soil conditions. We measured the leaf width (leaf size) and calculated fluctuating asymmetry (FA), coefficient of variation within and among individuals (CV_intra and CV_inter), and plasticity (PI_rel) in leaf size at days 30, 50, and 70 of plant growth, to analyze the correlations among these variables in response to density and soil conditions, at each of or across all growth stages. Results showed increased density led to lower leaf FA, CV_intra, and PI_rel and higher CV_inter in fertile soil. A positive correlation between FA and PI_rel occurred in infertile soil, while correlations between CV_inter and PI_rel and between CV_inter and CV_intra were negative at high density and/or in fertile soil, with nonsignificant correlations among them in other cases. Results suggested the complexity of responses of developmental instability, variability, and canalization in leaf size, as well as their relationships, which depend on the strength of stresses. Intense aboveground competition that accelerates the decrease in leaf size (leading to lower plasticity) will be more likely to reduce developmental instability, variability, and canalization in leaf size. Increased developmental instability and intra‐ and interindividual variability should be advantageous and facilitate adaptive plasticity in less stressful conditions; thus, they are more likely to positively correlate with plasticity, whereas developmental stability and canalization with lower developmental variability should be beneficial for stabilizing plant performance in more stressful conditions, where they tend to have more negative correlations with plasticity.     

Trait variability and stress: canalization, developmental stability and the need for a broad approach

Trait variability (particularly fluctuating asymmetry) may provide a general measure of environmental stress applicable across taxa but consistent empirical support is lacking. Historically, stress effects were considered to act independently on trait canalization, developmental noise and trait size. However, in trait comparisons these processes are often assumed to be associated. Here we reconsider this issue and implications for detecting stress effects using trait variability. Published studies that consider multiple environments report little association between the effects of environmental variation on trait canalization and on developmental noise measured as fluctuating asymmetry, sug-gesting that environmental effects often act independently on these processes. To further test the usefulness of trait variability as an indicator of stress, comparisons across environ-ments should take a broad approach and report on several measures of trait variability, rather than focusing on only one index of fluctuating asymmetry as is commonly done.     

EVOLUTION OF VARIATION AND VARIABILITY UNDER FLUCTUATING,STABILIZING, AND DISRUPTIVE SELECTION

How variation and variability (the capacity to vary) may respond to selection remain open questions. Indeed, effects of different selection regimes on variational properties, such as canalization and developmental stability are under debate. We analyzed the patterns of among‐ and within‐individual variation in two wing‐shape characters in populations of Drosophila melanogaster maintained under fluctuating, disruptive, and stabilizing selection for more than 20 generations. Patterns of variation in wing size, which was not a direct target of selection, were also analyzed. Disruptive selection dramatically increased phenotypic variation in the two shape characters, but left phenotypic variation in wing size unaltered. Fluctuating and stabilizing selection consistently decreased phenotypic variation in all traits. In contrast, within‐individual variation, measured by the level of fluctuating asymmetry, increased for all traits under all selection regimes. These results suggest that canalization and developmental stability are evolvable and presumably controlled by different underlying genetic mechanisms, but the evolutionary responses are not consistent with an adaptive response to selection on variation. Selection also affected patterns of directional asymmetry, although inconsistently across traits and treatments.     

Genome-wide deficiency mapping of the regions responsible for temporal canalization of the developmental processes of Drosophila melanogaster

Developmental processes of organisms are programmed to proceed in a finely regulated manner and finish within a certain period of time depending on the ambient environmental conditions. Therefore, variation in the developmental period under controlled genetic and environmental conditions indicates innate instability of the developmental process. In this study, we aimed to determine whether a molecular machinery exists that regulates the canalization of the developmental period and, if so, to test whether the same mechanism also stabilizes a morphological trait. To search for regions that influence the instability of the developmental period, we conducted genome-wide deficiency mapping with 441 isogenic deficiency strains covering 65.5% of the Drosophila melanogaster genome. We found that 11 independent deficiencies significantly increased the instability of the developmental period and 5 of these also significantly increased the fluctuating asymmetry of wing shape although there was no significant correlation between the instabilities of developmental period and wing shape in general. These results suggest that canalization processes of the developmental period and morphological traits are at least partially independent. Our findings emphasize the potential importance of temporal variation in development as an indicator of developmental stability and canalization and provide a novel perspective for understanding the regulation of phenotypic variability.     

How accurate is the phenotype? – An analysis of developmental noise in a cotton aphid clone

Background  

The accuracy by which phenotype can be reproduced by genotype potentially is important in determining the stability, environmental sensitivity, and evolvability of morphology and other phenotypic traits. Because two sides of an individual represent independent development of the phenotype under identical genetic and environmental conditions, average body asymmetry (or "fluctuating asymmetry") can estimate the developmental instability of the population. The component of developmental instability not explained by intrapopulational differences in gene or environment (or their interaction) can be further defined as internal developmental noise. Surprisingly, developmental noise remains largely unexplored despite its potential influence on our interpretations of developmental stability, canalization, and evolvability. Proponents of fluctuating asymmetry as a bioindicator of environmental or genetic stress, often make the assumption that developmental noise is minimal and, therefore, that phenotype can respond sensitively to the environment. However, biologists still have not measured whether developmental noise actually comprises a significant fraction of the overall environmental response of fluctuating asymmetry observed within a population.     

Fluctuating asymmetry--indicator of what?

In a population the optimal phenotype is promoted by buffering mechanisms that keep inter- and intra-individual variation low. A link exists between canalization, that controls phenotypic variation, and developmental stability, mostly measured as fluctuating asymmetry of bilateral traits (FA). Both types of variation are associated with the functional importance of a trait, and both are increased by stress of various kinds. But there are also several instances of non-congruence. The concept of developmental stability has been found elusive, and low FA is not the unambiguous measure of well being and good genes that has been claimed. It can be concluded that developmental stability is partly governed by specific, as yet unknown, molecular processes.     

Developmental Stability of DROSOPHILA MELANOGASTER under Artificial and Natural Selection in Constant and Fluctuating Environments

Populations of Drosophila melanogaster in constant 25° and fluctuating 20/29° environments showed increases in developmental stability, indicated by decreases in bilateral asymmetry of sterno-pleural chaeta number. In both environments, rates of decrease in asymmetry were greater under natural selection (control lines) than under artificial stabilizing selection. Overall mean asymmetry was greater in the fluctuating environment.—There was no evidence that decreased asymmetry was due to heterozygosity, and the decline in asymmetry was not explained by the decline in chaeta number in the lines under only natural selection. However, the decline was consistent with changes in total phenotypic variance and environmental variance.—The divergence between lines after 39 generations of selection was seen in differences in asymmetry and also in the genotype-environment interaction expressed in cross-culturing experiments.     

GEOMETRIC MORPHOMETRICS OF DEVELOPMENTAL INSTABILITY: ANALYZING PATTERNS OF FLUCTUATING ASYMMETRY WITH PROCRUSTES METHODS

Although fluctuating asymmetry has become popular as a measure of developmental instability, few studies have examined its developmental basis. We propose an approach to investigate the role of development for morphological asymmetry by means of morphometric methods. Our approach combines geometric morphometrics with the two-way ANOVA customary for conventional analyses of fluctuating asymmetry and can discover localized features of shape variation by examining the patterns of covariance among landmarks. This approach extends the notion of form used in studies of fluctuating asymmetry from collections of distances between morphological landmarks to an explicitly geometric concept of shape characterized by the configuration of landmarks. We demonstrate this approach with a study of asymmetry in the wings of tsetse flies (Glossina palpalis gambiensis). The analysis revealed significant fluctuating and directional asymmetry for shape as well as ample shape variation among individuals and between the offspring of young and old females. The morphological landmarks differed markedly in their degree of variability but multivariate patterns of landmark covariation identified by principal component analysis were generally similar between fluctuating asymmetry (within-individual variability) and variation among individuals. Therefore there is no evidence that special developmental processes control fluctuating asymmetry. We relate some of the morphometric patterns to processes known to be involved in the development of fly wings.     

Bite Force Performance,Fluctuating Asymmetry and Antisymmetry in the Mandible of Inbred and Outbred Wild-Derived Strains of Mice (<Emphasis Type="Italic">Mus musculus domesticus</Emphasis>)

Developmental instability, as measured by fluctuating asymmetry is generally considered to increase with genetic and environmental stresses. Few studies have, however, addressed the role of asymmetry in altering organism performance. Here, we measured bite force performance in three strains of inbred and outbred mice derived from wild ancestors. We quantified size and shape directional, and fluctuating asymmetry, as well as inter-individual variation of their mandibles using geometric morphometrics. We also developed a way to estimate shape antisymmetry, to filter it out of the fluctuating asymmetry component. Contrary to our expectations, we found no significant link between bite force and asymmetry levels. Inbreeding did not produce any clear and significant increase or decrease in neither inter-individual variance, nor fluctuating asymmetry. Furthermore, fluctuating asymmetry levels were unrelated to inter-individual variance levels, although these two types of variation affected the same areas of the mandible. We did not highlight any impact of inbreeding depression on bite force. Fluctuating asymmetry was reduced in the mandible, which we argue may be linked to its functional relevance. We found some significant but very reduced antisymmetry possibly linked to lateralization. This lateralization did not relate to any bite force difference. Our results show that neither inbreeding, nor asymmetry (combining fluctuating, directional asymmetry and antisymmetry) significantly affect bite force performance in mice, and that despite affecting the same morphological regions, developmental stability and canalization are independent.     

Phenotypic Buffering in a Monogenean: Canalization and Developmental Stability in Shape and Size of the Haptoral Anchors of Ligophorus cephali (Monogenea: Dactylogyridae)

Phenotypic variation results from the balance between sources of variation and counteracting regulatory mechanisms. Canalization and developmental stability are two such mechanisms, acting at two different levels of regulation. The issue of whether or not they act concurrently as a common developmental buffering capacity has been subject to debate. We used geometric morphometrics to quantify the mechanisms that guarantee phenotypic constancy in the haptoral anchors of Ligophorus cephali. Canalization and developmental stability were appraised by estimating inter- and intra-individual variation, respectively, in size and shape of dorsal and ventral anchors. The latter variation was estimated as fluctuating asymmetry (FA) between anchor pairs. The general-buffering-capacity hypothesis was tested by two different methods based on correlations and Principal Components Analyses of the different components of size and shape variation. Evidence for FA in the dorsal and ventral anchors in both shape and size was found. Our analyses supported the hypothesis of a general developmental buffering capacity. The evidence was more compelling for shape than for size and, particularly, for the ventral anchors than for the dorsal ones. These results are in line with previous studies of dactylogyrids suggesting that ventral anchors secure a firmer, more permanent attachment, whereas dorsal anchors are more mobile. Because fixation to the host is crucial for survival in ectoparasites, we suggest that homeostatic development of the ventral anchors has been promoted to ensure the morphological constancy required for efficient attachment. Geometric morphometrics can be readily applied to other host-monogenean models, affording not only to disentangle the effects of canalization and developmental stability, as shown herein, but to further partition the environmental and genetic components of the former.     

Developmental stability and canalization of limb bones of brown haresLepus europaeus with varying levels of heterozygosity

We have studied fluctuating asymmetry (FA), as indicator of developmental stability, and between-individual variation, as surrogate of developmental canalization (DC), in long bones (humerus, ulna, radius, femur, tibia) of 72 wild-living adult-sized brown haresLepus europaeus Pallas, 1778 with variable individual heterozygosity (H).H was calculated from 13 polymorphic allozyme loci. According to the “over-dominance hypothesis”, we expected increased developmental stability and canalization at higherH-levels. But at the individual level we did not find any significant correlation between overall FA (FA_I) andH. Also, standard deviations (SD) of mean length (over both body sides) of bones did not differ between individuals from two intentionally created groups of hares, namely one with high and one with lowH. FA-indices and variances of FA-indices of bone lengths did not differ significantly when compared between two intentionally created groups of hares with high and low SD of bone lengths, respectively. These latter findings suggest that developmental stability and DC are two separate or partly separate mechanisms of developmental homeostasis in the studied appendicular skeleton, and thatH has no traceable effect on develop-mental homeostasis. If there is still such an effect, it should be clearly smaller than a possibly combined effect of (presently uncontrolled) environmental stressors.     

Independence between developmental stability and canalization in the skull of the house mouse

The relationship between the two components of developmental homeostasis, that is canalization and developmental stability (DS), is currently debated. To appraise this relationship, the levels and morphological patterns of interindividual variation and fluctuating asymmetry were assessed using a geometric morphometric approach applied to the skulls of laboratory samples of the house mouse. These three samples correspond to two random-bred strains of the two European subspecies of the house mouse and their F1 hybrids. The inter- and intraindividual variation levels were found to be smaller in the hybrid group compared to the parental ones, suggesting a common heterotic effect on skull canalization and DS. Both buffering mechanisms might then depend on the same genetic condition, i.e. the level of heterozygosity. However, related morphological patterns did not exhibit any congruence. In contradiction with previous studies on insect wing traits, we therefore suggest that canalization and DS may not act on the same morphological characters. The fact that this discrepancy could be related to the functional importance of the symmetry of the characters under consideration is discussed in the light of our knowledge of the genetic bases of both components of developmental homeostasis.     

Canalization and developmental instability of the fetal skull in a mouse model of maternal nutritional stress

Nutritional imbalance is one of the main sources of stress in both extant and extinct human populations. Restricted availability of nutrients is thought to disrupt the buffering mechanisms that contribute to developmental stability and canalization, resulting in increased levels of fluctuating asymmetry (FA) and phenotypic variance among individuals. However, the literature is contradictory in this regard. This study assesses the effect of prenatal nutritional stress on FA and among‐individual variance in cranial shape and size using a mouse model of maternal protein restriction. Two sets of landmark coordinates were digitized in three dimensions from skulls of control and protein restricted specimens at E17.5 and E18.5. We found that, by the end of gestation, maternal protein restriction resulted in a significant reduction of skull size. Fluctuating asymmetry in size and shape exceeded the amount of measurement error in all groups, but no significant differences in the magnitude of FA were found between treatments. Conversely, the pattern of shape asymmetry was affected by the environmental perturbation since the angles between the first eigenvectors extracted from the covariance matrix of shape asymmetric component of protein restricted and control groups were not significantly different from the expected for random vectors. In addition, among‐individual variance in cranial shape was significantly higher in the protein restricted than the control group at E18.5. Overall, the results obtained from a controlled experiment do not support the view of fluctuating asymmetry of cranial structures as a reliable index for inferring nutritional stress in human populations. Am J Phys Anthropol 154:544–553, 2014. © 2014 Wiley Periodicals, Inc.     

Symmetry breaking in interspecific Drosophila hybrids is not due to developmental noise

Hybrids from crosses of different species have been reported to display decreased developmental stability when compared to their pure species, which is conventionally attributed to a breakdown of coadapted gene complexes. Drosophila subobscura and its close relative D. madeirensis were hybridized in the laboratory to test the hypothesis that genuine fluctuating asymmetry, measured as the within-individual variance between right and left wings that results from random perturbations in development, would significantly increase after interspecific hybridization. When sires of D. subobscura were mated to heterospecific females following a hybrid half-sib breeding design, F1 hybrid females showed a large bilateral asymmetry with a substantial proportion of individuals having an asymmetric index larger than 5% of total wing size. Such an anomaly, however, cannot be plainly explained by an increase of developmental instability in hybrids but is the result of some aberrant developmental processes. Our findings suggest that interspecific hybrids are as able as their parents to buffer developmental noise, notwithstanding the fact that their proper bilateral development can be harshly compromised. Together with the low correspondence between the co-variation structures of the interindividual genetic components and the within-individual ones from a Procrustes analysis, our data also suggest that the underlying processes that control (genetic) canalization and developmental stability do not share a common mechanism. We argue that the conventional account of decreased developmental stability in interspecific hybrids needs to be reappraised.