Evolutionary history shapes the association between developmental instability and population‐level genetic variation in three‐spined sticklebacks

Developmental instability (DI) is the sensitivity of a developing trait to random noise and can be measured by degrees of directionally random asymmetry [fluctuating asymmetry (FA)]. FA has been shown to increase with loss of genetic variation and inbreeding as measures of genetic stress, but associations vary among studies. Directional selection and evolutionary change of traits have been hypothesized to increase the average levels of FA of these traits and to increase the association strength between FA and population‐level genetic variation. We test these two hypotheses in three‐spined stickleback (Gasterosteus aculeatus L.) populations that recently colonized the freshwater habitat. Some traits, like lateral bone plates, length of the pelvic spine, frontal gill rakers and eye size, evolved in response to selection regimes during colonization. Other traits, like distal gill rakers and number of pelvic fin rays, did not show such phenotypic shifts. Contrary to a priori predictions, average FA did not systematically increase in traits that were under presumed directional selection, and the increases observed in a few traits were likely to be attributable to other factors. However, traits under directional selection did show a weak but significantly stronger negative association between FA and selectively neutral genetic variation at the population level compared with the traits that did not show an evolutionary change during colonization. These results support our second prediction, providing evidence that selection history can shape associations between DI and population‐level genetic variation at neutral markers, which potentially reflect genetic stress. We argue that this might explain at least some of the observed heterogeneities in the patterns of asymmetry.     

Fluctuating asymmetry in certain morphological traits in laboratory populations of Drosophila ananassae.

Fluctuating asymmetry (FA, subtle random deviations from perfect bilateral symmetry) is often used as a measure of developmental instability (DI), which results from perturbations in developmental pathways caused by genetic or environmental stressors. During the present study, we estimated FA in 5 morphological traits, viz. wing length (WL), wing to thorax ratio (W:T), sternopleural bristle number (SBN), sex-comb tooth number (SCTN), and ovariole number (ON) in 18 laboratory populations of Drosophila ananassae. FA levels of measured traits differed significantly among populations except for SBN (in males and females) and W:T ratio (in females). Positional fluctuating asymmetry (PFA), a sensitive measure of DI, also varied significantly among the populations for SBN in females and SCTN in males. Interestingly, both males and females were similar for nonsexual traits. However, when FA across all traits (sexual and nonsexual) was combined into a single composite index (CFA), significant differences were found for both populations and sexes. Males showed higher CFA values than females, suggesting that males are more prone to developmental perturbations. The magnitude of FA differed significantly among traits, being lowest for nonsexual traits (SBN, WL, W:T ratio) and highest for sexual traits (SCTN and ON). The trait size of sexual traits (SCTN and ON) was positively correlated with their asymmetry. The possible reasons for variation in FA both among traits and among populations, and the usefulness of FA as an indicator of developmental stress and phenotypic quality in D. ananassae are discussed.     

Impact of temperature shifts on the joint evolution of seed dormancy and size

Seed dormancy and size are two important life‐history traits that interplay as adaptation to varying environmental settings. As evolution of both traits involves correlated selective pressures, it is of interest to comparatively investigate the evolution of the two traits jointly as well as independently. We explore evolutionary trajectories of seed dormancy and size using adaptive dynamics in scenarios of deterministic or stochastic temperature variations. Ecological dynamics usually result in unbalanced population structures, and temperature shifts or fluctuations of high magnitude give rise to more balanced ecological structures. When only seed dormancy evolves, it is counter‐selected and temperature shifts hasten this evolution. Evolution of seed size results in the fixation of a given strategy and evolved seed size decreases when seed dormancy is lowered. When coevolution is allowed, evolutionary variations are reduced while the speed of evolution becomes faster given temperature shifts. Such coevolution scenarios systematically result in reduced seed dormancy and size and similar unbalanced population structures. We discuss how this may be linked to the system stability. Dormancy is counter‐selected because population dynamics lead to stable equilibrium, while small seeds are selected as the outcome of size‐number trade‐offs. Our results suggest that unlike random temperature variation between generations, temperature shifts with high magnitude can considerably alter population structures and accelerate life‐history evolution. This study increases our understanding of plant evolution and persistence in the context of climate changes.     

Effects of maternal body morphology, morning sickness, gestational diabetes and hypertension on fluctuating asymmetry in young women

The magnitude of fluctuating asymmetry (FA)—an indicator of genetic and phenotypic quality—can be affected by genetic perturbations, environmental stressors, and maternal effect (maternal age, diseases, dietary deficiency). Maternal effect on human FA has been typically investigated in newborns or very young children. There are no studies investigating whether maternal effect can disrupt developmental mechanisms responsible for the secondary sexual traits that are manifested at adulthood under the influence of steroid hormones. We investigated the effect of maternal degree of obesity, gestational diabetes and hypertension, and morning sickness on the magnitude of FA in nonsexual traits as well as asymmetric thigh circumference—a sexually differentiated trait—in adult daughters. Results revealed that gestational diabetes and hypertension and maternal obesity are positively associated with FA in nonsexual traits. FA in nonsexual traits was not associated with morning sickness; however, the FA in the sexual trait (thigh circumference) was positively related to third-trimester morning sickness. Fluctuating asymmetries of nonsexual traits and thigh circumference were significantly correlated. This preliminary study demonstrates a maternal effect on adult daughters' developmental instability as measured by sexual and nonsexual traits.     

Patterns and drivers of intraspecific variation in avian life history along elevational gradients: a meta‐analysis

Elevational gradients provide powerful natural systems for testing hypotheses regarding the role of environmental variation in the evolution of life‐history strategies. Case studies have revealed shifts towards slower life histories in organisms living at high elevations yet no synthetic analyses exist of elevational variation in life‐history traits for major vertebrate clades. We examined (i) how life‐history traits change with elevation in paired populations of bird species worldwide, and (ii) which biotic and abiotic factors drive elevational shifts in life history. Using three analytical methods, we found that fecundity declined at higher elevations due to smaller clutches and fewer reproductive attempts per year. By contrast, elevational differences in traits associated with parental investment or survival varied among studies. High‐elevation populations had shorter and later breeding seasons, but longer developmental periods implying that temporal constraints contribute to reduced fecundity. Analyses of clutch size data, the trait for which we had the largest number of population comparisons, indicated no evidence that phylogenetic history constrained species‐level plasticity in trait variation associated with elevational gradients. The magnitude of elevational shifts in life‐history traits were largely unrelated to geographic (altitude, latitude), intrinsic (body mass, migratory status), or habitat covariates. Meta‐population structure, methodological issues associated with estimating survival, or processes shaping range boundaries could potentially explain the nature of elevational shifts in life‐history traits evident in this data set. We identify a new risk factor for montane populations in changing climates: low fecundity will result in lower reproductive potential to recover from perturbations, especially as fewer than half of the species experienced higher survival at higher elevations.     

FLUCTUATING ASYMMETRY: AN EPIGENETIC MEASURE OF STRESS

(1) Fluctuating asymmetry (FA) is a useful trait for monitoring stress in the laboratory and in natural environments.
(2) Both genomic and environmental changes can increase FA which represents a deterioration in developmental homeostasis apparent in adult morphology. Genetic perturbations include intense directional selection and certain specific genes. Environmental perturbations include temperature extremes in particular, protein deprivation, audiogenic stress, and exposure to pollutants.
(3) There is a negative association between FA and heterozygosity in a range of taxa especially fish, a result consistent with FA being a measure of fitness.
(4) Scattered reports on non-experimental populations are consistent with experiments under controlled laboratory conditions. FA tends to increase as habitats become ecologically marginal; this includes exposure to environmental toxicants.
(5) In our own species, FA of an increasing range of traits has been related to both environmental and genomic stress.
(6) Domestication increases FA of the strength of homologous long bones of vertebrate species due to a relaxation of natural selection.
(7) FA levels are paralleled by the incidence of skeletal abnormalities in stressful environments.
(8) Increased FA is a reflection of poorer developmental homeostasis at the molecular, chromosomal and epigenetic levels.     

Hand asymmetry does not relate to key life history traits in post-menopausal contemporary Finnish women

Associations between fluctuating asymmetry (FA, a putative marker of developmental instability, DI) and life history traits have received a great deal of attention in the non-human literature. However, the patterns found are very heterogeneous and generalizations are difficult to make. In humans, only a few studies have related FA to life histories and fitness. In this paper we study such relationships using hand FA and several key life history traits in 209 post-menopausal Finnish women born between 1946 and 1958. Asymmetry measurements were based on scans of the hands and the life histories of these women were collected using questionnaires. No significant associations were detected and trends were opposite to expectations. We did find evidence for directional asymmetry, as traits in the right hand were larger on average. This may be due to handedness, questioning the usefulness of hand FA as a measure of DI. We conclude that future studies in humans should carefully examine the usefulness of traits as measures of DI.     

Genetic and environmental influence on the asymmetry of dermatoglyphic traits

Fluctuating asymmetry (FA) is defined as random deviations from bilateral symmetry of the body. Thus, its magnitude is often used to evaluate developmental homeostasis. In this study we evaluate the following hypotheses: 1) FA of dermatoglyphic traits has a significant genetic component; 2) prenatal maternal environment (PME) has a significant effect on the FA of dermatoglyphic traits in developmentally healthy individuals; and 3) genetic or environmental factors affect FA on organismal or systemic levels. Therefore, their effect is better seen in composite scores of FA rather than in FA indices for single traits. We analyzed 15 dermatoglyphic traits from 140 pairs of monozygous twins, 120 pairs of dizygous twins, and 106 pairs of mothers and daughters. All individuals were developmentally healthy. The influence of genetic and environmental factors on FA was evaluated by analysis of variance and regression analysis. For a majority of the traits in our study, FA showed significant but weak heritabilities, with values falling within the 0.20-0.35 range. None of the traits taken separately demonstrated the effect of PME on FA to be significantly greater than zero. The composite score of FA tended to have greater heritability values than individual traits. One of them, obtained in principal components analysis, showed a significant PME effect, supporting the hypothesis that FA is a systemic property.     

Morphological asymmetry of insular freshwater populations of threespine stickleback

Fluctuating asymmetry (FA), random deviations from perfect symmetry in a bilateral organism, has been widely used as a proxy for developmental instability in stressed populations. In order to test the utility of FA of resident freshwater threespine stickleback (Gasterosteus aculeatus) as a biomonitoring tool for contaminated sites, we compared levels of asymmetry of seven morphological traits of threespine stickleback collected from lakes at three islands with a history of military contamination and three islands with no military history, in the Aleutian Archipelago, Alaska. Traits examined include eye diameter, operculum width, pectoral fin ray number, pectoral fin width, lateral plate number, lateral plate length, and pelvic spine length. All morphometric traits demonstrated some degree of FA or directional asymmetry (DA), but the military history of a lake was not a predictor of the degree or type of asymmetry. Overall, the patterns of asymmetry were similar for all traits, irrespective of military contamination at a lake. Our results demonstrate that the suite of threespine stickleback traits measured are not suitable for examination of FA as a proxy for aquatic pollution in this region. DA also does not appear to be suitable as an indicator of aquatic pollution, but may instead be driven by local ecological factors such as predation.     

Multilevel Control of Organelle DNA Sequence Length in Plants

We have compared the length of noncoding organelle DNA spacers in a broad sample of plant species characterized by different life history traits to test hypotheses regarding the nature of the mechanisms driving changes in their size. We first demonstrate that the spacers do not evolve at random in size but have experienced directional evolutionary trends during plant diversification. We then study the relationships between spacer lengths and other molecular features and various species attributes by taking into account population genetic processes acting within cell lineages. Comparative techniques are used to test these relationships while controlling for species phylogenetic relatedness. The results indicate that spacer length depends on mode of organelle transmission, on population genetic structure, on nucleotide content, on rates of molecular evolution, and on life history traits, in conformity with predictions based on a model of intracellular competition among replicating organelle genomes. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Natural genetic variation in fluctuating asymmetry of wing shape in Drosophila melanogaster

Fluctuating asymmetry (FA), defined as random deviation from perfect symmetry, has been used to assay the inability of individuals to buffer their developmental processes from environmental perturbations (i.e., developmental instability). In this study, we aimed to characterize the natural genetic variation in FA of wing shape in Drosophila melanogaster, collected from across the Japanese archipelago. We quantified wing shapes at whole wing and partial wing component levels and evaluated their mean and FA. We also estimated the heritability of the mean and FA of these traits. We found significant natural genetic variation in all the mean wing traits and in FA of one of the partial wing components. Heritability estimates for mean wing shapes were significant in two and four out of five wing traits in males and females, respectively. On the contrary, heritability estimates for FA were low and not significant. This is a novel study of natural genetic variation in FA of wing shape. Our findings suggest that partial wing components behave as distinct units of selection for FA, and local adaptation of the mechanisms to stabilize developmental processes occur in nature.     

Dimorphisms and fluctuating asymmetry in the forceps of male earwigs

Male dimorphisms are particularly conspicuous examples of the alternative reproductive strategies employed within some species. Such dimorphisms are thought to exist as genetic polymorphisms under ESS conditions, or to be conditional strategies where exogenous conditions determine the adult body plan. Fluctuating asymmetry (FA) is currently considered to be a fitness correlate of significant use in interpreting the functional significance of secondary sexual characteristics. In particular, negative slopes of FA on trait size are thought to arise in traits whose expression is dependent on condition. We measured forceps lengths and asymmetries in 2 island populations of the European earwig Forficula auricularia and Museum specimens of 5 other earwig (Dermaptera, Forficulidae) species from different genera, that appeared to be dimorphic. In a detailed study of Forficula auricularia we found a significant fit to a statistical model for the identification of dimorphisms and, for all species examined, morphs differed in the slope and/or elevation of the allometric relationship between body size and forcep length. Possible determinates of male dimorphisms are suggested from the data. Contrary to expectation, FA was not found to be greater in the minor morphs. Negative relationships between FA and forceps length were absent in both morphs of species examined from museum collections. Of the two island populations of Forficula auricularia, the smaller and more isolated population had higher FA and a negative relationship between FA and forceps length in the major morph. We discuss these patterns in the light of recent theories of FA and honest signalling.     

Maternal and paternal contributions to egg size and egg number variation in the blackfin pearl killifish <Emphasis Type="Italic">Austrolebias nigripinnis</Emphasis>

Reproductive effort, egg number and egg size are traditionally considered to be ‘female’ life history traits. However, females often adjust the amount of resources allocated to reproduction depending on their mate, causing male environmental effects on life history traits. If females respond to male traits which are genetically variable, then male environmental effects contain indirect genetic effects. Estimates of how much of the total variation in life history traits originates from female effects versus male environmental effects, seems mostly lacking. We have investigated variation in rates of egg production and in egg size in the annual Argentinian blackfin pearl killifish Austrolebias nigripinnis, in a crossed design where males were exchanged repeatedly between females. Our analysis of phenotypic variance components of reproductive effort, egg size and egg number indicates that the amount of variation contributed by male environmental effects is equal (egg size, reproductive effort) or larger (egg number) than that between females. For egg size and number, we find that male environmental effects consist of a male random effect representing the average response of females to male phenotype, plus a female-male interaction term. This term can be understood as the deviation from the population mean of an individual female’s response. For reproductive effort, we find that the male environmental effect consists of an interaction term only. Random effects on egg size and number additionally vary in magnitude depending on the weekday where we collected eggs, probably due to cyclic variation in experimental conditions. Since we find that both male phenotype and environmental conditions affect egg size and number as determined by females, our results suggest that selection on these life history traits will be frequency-dependent.     

Repeatability of size and fluctuating asymmetry of antler characteristics in red deer (Cervus elaphus) during ontogeny

Fluctuating asymmetry (FA) has been suggested as a measure of the sensitivity of development to a wide array of genetic and environmental stresses. It has been also suggested that antlers in red deer could be important during social and rutting displays. We used antler measurements of 51 males that were measured over subsequent seasons, from 3–8 years of age, and analysed three antler traits: antler weight, length, and the number of antler tines (antler size). We calculated absolute and relative FA. All three size traits were highly significantly intercorrelated. By contrast to this, the FA of the three traits, did not show such relationships. With increasing age, antler size and FA also increased. When testing the repeatability of FA and antler size, there was a principal difference in the pattern between FA and antler size, with the latter being much more consistent than the former. This suggests that antler size, not FA, may be a good predictor of the bearer's quality in mate selection. This fits well with the good-genes hypothesis that the development of extravagant secondary sexual characters can be an honest advertisement of heritable male quality.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 215–226.     

Fluctuating asymmetry of meristic traits: an isofemale line analysis in an invasive drosophilid, <Emphasis Type="Italic">Zaprionus indianus</Emphasis>

Metric (e.g., body size) and meristic (e.g., bristle number) traits are of general use in quantitative genetic studies, and the phenotypic variance is subdivided into a genetic and a non-genetic environmental component. The non-genetic variance may have two origins: a common garden effect between individuals and a developmental instability within the same individual. Developmental instability may be studied by considering the fluctuating asymmetry (FA) between the two sides of the body. The isofemale line technique is a convenient method for investigating the architecture of natural populations but has been rarely implemented for investigating FA. In this paper, we use this experimental design for analyzing four meristic traits in eight populations of the cosmopolitan Zaprionus indianus. A study of the correlation between left and right side of each line revealed that almost 90% of the variability was due to a developmental noise, while a much higher correlation among the means of the lines from the same population was observed. A slight trend toward a directional asymmetry was observed: more thoracic bristles on the left side. Four kinds of indices, scaled or non-scaled to the mean were used for comparing the different traits. Unscaled values (mean absolute values or standard deviation of each line) revealed a linear increase with the means. Interestingly the results of ovariole number were included in the same regression. With the scaled indices (mean absolute divided by each individual value or stadard deviation devided by the mean), the differences among traits were considerably decreased, but still remained significant. The mean FA of the various traits were not correlated, suggesting that each trait harbors its own developmental stability. The CVs of FA were high with a magnitude similar to those of the trait themselves, slightly less than 10%. Finally, even with the isofemale line design, which is a powerful means for unravelling slight genetic variations, we did not to find any clear indication of a genetic component of FA under the optimal environmental conditions used in this study.     

Environmental stress increases skeletal fluctuating asymmetry in the moor frog Rana arvalis

Whether fluctuating asymmetry (FA) provides a useful metric indicator of the degree of environmental stress experienced by populations is still a contentious issue. We investigated whether the degree of FA in skeletal elements is useful in elucidating the degree of environmental stress experienced by frog populations, and further, tested the proposition that a trait’s sensitivity to stress—as reflected in the degree of FA—is related to the degree of directional selection experienced by the given trait. We compared the degree of FA in four bilateral skeletal elements of male and female moor frogs (Rana arvalis) originating from low (acidified) and neutral pH populations. While the degree of uncorrected FA was unrelated to the degree of acidity, the growth rate and age of the individuals, the size-corrected FA was significantly higher in low than in neutral pH populations and decreased with individual ages and growth rates. In addition, both measures of FA were significantly higher in males and in particular in traits presumably under high sexual selection as indicated by the degree of sexual size dimorphism. All in all, the results indicate that individuals from acidified localities are smaller, younger and exhibit a significantly higher degree of FA than individuals from neutral pH populations. These results constitute the first assessment of FA in amphibians and suggest that the degree of FA in skeletal traits can be a useful indicator of the degree of environmental stress experienced by amphibian populations.     

Genetic analysis of bilateral dermatoglyphic asymmetry in twins and their parents

The data for this study were collected on 64 twin pairs (30 MZ and 34 DZ) and their 128 parents. Two following hypotheses were evaluated: 1. Bilateral asymmetry is significantly genetically controlled; 2. The twinning phenomenon would affect the magnitude of bilateral asymmetry. The results revealed no statistically significant differences between mean values of MZ and DZ twins and their parents for the majority of the traits. Significant differences were recorded for only 6 of 96 comparisons (6%). Analysis of variance revealed separated sources of MZ, DZ and singleton variance. F-ratios, contrasting variances between different groups were significant for 26 of 96 comparisons (27%) showing heterogeneity of variance between zygosities and between twins and their parents. In addition, environmental covariance appeared to be larger for MZ than DZ with respect to directional asymmetry (DA) for all 16 traits and fluctuating asymmetry (FA) for 14 traits. These observations showed complex environmental determinism for bilateral asymmetry for the majority of dermatoglyphic traits. Significant genetic variance ratios (GVRs) were observed for four variables (25%) with respect to DA and three variables (18.75%) with respect to FA. All these significant GVRs were rendered insignificant because of evidence of greater environmental covariance for MZ twins, except possibly for DA for URC4.     

The quantitative genetics of fluctuating asymmetry: a comparison of two models

The genetic basis of fluctuating asymmetry (FA), a measure of random deviations from perfect bilateral symmetry, has been the subject of much recent work. In this paper we compare two perspectives on the quantitative genetic analysis of FA and directional asymmetry (DA). We call these two approaches the character-state model and the environmental responsiveness model. In the former approach, the right and left sides are viewed as separate traits whose genetic coupling is manifested by the genetic correlation. This model leads to the relationship, h2(DA) = h2[(1-rA)/(1-rp)), where h2 is the heritability of each component trait (assumed to be the same), rA and rp are the genetic and phenotypic correlations between traits, respectively. Simulation shows that, under this model, the heritability of FA is considerably less than that of DA, except when heritabilities are very close to zero. The environmental responsiveness model permits genetic variance in FA even when the genetic correlation between traits is + 1. Simulation shows that under this model the heritability of FA can be uncoupled from that of DA. The additive and nonadditive components of the component (right and left) traits, their DA and FA values are estimated using a diallel cross of seven inbred lines of the sand cricket, Gryllus firmus. Four leg measurements were made and both the individual DA and FA values and the compound measures DASUM and CFA estimated. The heritabilities of the compound measures are slightly larger than the individual estimates. Dominance variance is observed in the individual traits but predicted to be an even smaller component of the phenotypic variance than the additive genetic variance. The estimated values confirm this, although a previous study has demonstrated that dominance variance is present. Because the heritabilities of FA are generally larger than those of DA, which never exceed 0.02, the environmental responsiveness model is more consistent with the data than the character-state model. A review of other data suggests that both sources of variation might be found in some species.     

Fluctuating asymmetry in the otoliths of larval fish as an indicator of condition: conceptual and methodological aspects

Developmental instability, measured as fluctuating asymmetry (FA) in bilateral traits, has been used widely as an indicator of genetic or environmental stress in a variety of plant and animal taxa. FA arises as small deviations from perfect bilateral symmetry which reflect 'mistakes' in developmental processes resulting from the inability of the genotype to buffer itself effectively against environmental perturbations. Recently, it has been proposed that FA in the otoliths can be used as an indicator of condition in larval fish. This paper reviews the conceptual and methodological aspects of FA relevant to its potential use as a measure of well-being. Its simplicity makes FA an attractive tool to measure developmental precision and condition. However, there are several pitfalls, such as measuring error or potentially size dependence. Subtle asymmetries, i.e. between sides variation of a trait at the individual level, may not always be indicative of condition and should be interpreted with caution. The past-growth record of otoliths may provide a powerful means of studying the development of asymmetries at the level of the individual.     

Is phenotypic canalization involved in the decline of the endemic Aquilegia thalictrifolia? Rethinking relationships between fluctuating asymmetry and species conservation status

Fluctuating asymmetry (FA), the deviation from the normal symmetrical condition of a morphological trait having specific morphological symmetry, increases in response to environmental and genetic stress, is related to phenotypic plasticity and is considered a tool for monitoring a species conservation status. However, FA–stress relations are dependent on measured traits or species‐specific characteristics such as mating system and habitat. This study investigates the relationships between FA, genetic diversity, population size, density and individual fitness traits (plant height, fruit and seed set), in the endemic Aquilegia thalictrifolia, a mixed breeder that is declining, but maintaining high levels of heterozygosity. Leaf and flower FA and other traits were investigated in 10 populations of A. thalictrifolia, the whole species range. As a result, we found similar patterns of FA in leaves and flowers between populations, indicating a homogenous level of stress between populations that differed for other traits. FA and the other traits were not related, including heterozygosity. Heterozygosity was not related to individual fitness traits with the exception of plant height. In accordance with other studies, we found that the role of FA as a tool for assessing the conservation status of a species or population should be reconsidered. However, we conclude that a low level of FA should not automatically be considered an indicator of good conservation status or low level of stress, because in species that evolved in highly stable environments it may indicate a scarce ability to plastically respond to environmental changes, as a consequence of environmental and genetic canalization. Further investigation of this point is needed.