Development of fluctuating asymmetry in tail feathers of the barn swallow Hirundo rustica

Fluctuating asymmetry represents usually small, random deviations from symmetry in bilateral morphological characters. The ontogeny of asymmetry in morphological characters may reveal information about developmental processes in a general sense. I studied the development of fluctuating asymmetry in feather characters of the barn swallow Hirundo rustica, that are developed repeatedly during the single annual moult, with the following results. First, the side developing a larger feather was found to be partially biased, as demonstrated by one side consistently developing a larger feather under natural and experimentally induced growth episode events. Second, asymmetric feathers were found to consist of asymmetric daily growth increments, and the size of the increments developing under different environmental conditions were positively correlated. Third, fluctuating asymmetries of feathers developing under different environmental conditions were positively correlated, although the level of asymmetry was larger under adverse environmental conditions. Fourth, individual asymmetries in tail length and growth bar length were unrelated to the duration of the developmental period, although late growth increments were smaller and more symmetric than early increments. These observations suggest that fluctuating asymmetry partially arises as a consequence of a random bias in the feather follicles and differences in environmental conditions during ontogeny of feathers.     

Patterns of fluctuating asymmetry in flowers: Implications for sexual selection in plants

Characters in animals used in signalling and subjected to strong directional selection often demonstrate (i) an elevated level of fluctuating asymmetry (small random deviations from bilateral symmetry) and (ii) a negative relationship between the degree of individual fluctuating asymmetry and the size of a given character. We tested these two predictions in plants since flowers are subjected to strong directional selection and are involved in signalling to pollinators, whereas leaves are supposed not to be directly involved in signalling. The overall level of fluctuating asymmetry in a number of plant species with bilaterally or radially symmetric flowers was not generally higher in floral traits than in leaves. The level of fluctuating asymmetry in plants was sometimes significantly consistent within individuals. The absolute degree of individual fluctuating asymmetry in floral traits was generally negatively related to the size of the trait, while there was a positive relationship for leaves. The degree of individual fluctuating asymmetry in floral traits was marginally negatively related to the degree of individual fluctuating asymmetry in leaf traits. These patterns of fluctuating asymmetry in plants suggest that (i) the degree of asymmetry in flowers signals different aspects of quality than does the degree of asymmetry in leaves, and that (ii) fluctuating asymmetry in flowers often reflects the phenotypic quality of individual plants.     

Growth, survival and fluctuating asymmetry of Iceland scallops in a test of density-dependent growth in a natural bed

We report an experiment designed to test for overpopulation in an Iceland scallop, Chlamys islandica (O.F. Müller), slow-growing bed. Scallops were installed in pearl nets at the site of the scallop bed and in a nearby unpopulated site, near the bottom and far from the bottom. With this set-up, all groups, except that one near the bottom inside the bed, were free from potential overpopulation effects. In addition, there were two stocking densities to test for containment effects.Shell growth was higher at 2.0 m above the bottom, outside the scallop bed, than at the three other site and height combinations, which were not significantly different from each other. There was a borderline effect of site on soft tissue growth, which was probably slower at the donor site. We conclude that there was no evidence of overpopulation in the scallop bed. On both sites, soft tissue growth was slowest near the bottom, irrespective of group size, intermediate at 2.0 m height, high population density, and fastest at 2.0 m height, low population density. Survivorship was lower near the bottom, but was independent of site and of group size. Available data showed no sustained vertical patterns in phytoplankton concentration in the water column. These results suggest that food depletion occurred in the pearl nets, but that density-independent factors dominated density-dependent factors in the pearl nets near the bottom. Likely explanations involve the interaction between containment effects and current speed variations in the benthic boundary layer. Survivorship decreased with fluctuating asymmetry of the ears of the shells. Fluctuating asymmetry, therefore, may provide a means of including individual effects in growth experiments and forecasting the ability of spat to resist density-independent mortality agents.     

Patterns of fluctuating asymmetry in beetle horns: no evidence for reliable signaling

Negative relations between trait size and levels of fluctuatingasymmetry in secondary sexual traits have been claimed to beindicative of honest signaling of male quality. Comparativestudies of beetle horns have been used to illustrate the requirednegative relation between trait size and asymmeiry However,such studies may be confounded by measurement error or samplingbias due to population differences or differences within speciesin the phenotypic expression of hornedness. We examined thepatterns of fluctuating asymmetry within two species of hornedbeetle. We found that, in agreement with theory, horns exhibitgreater asymmetry than naturally selected traits. However, wefound a strong positive relation between horn size and asymmetryin Onthophagus taurs, a species with male dimorphisms, and aflat relation in Bubas bison, a species with continuous variationin horn size. We suggest that these differences may reflectfunctional differences in horns. We conclude that patterns ofasymmetry in horned beetles do not support the notion of honestsignaling.     

Birth order and fluctuating asymmetry: a first look

We investigated the hypothesis that maternal immunoreactivity to male-specific features of the foetus can increase developmental instability. We predicted that the participants' number of older brothers would be positively related to the fluctuating asymmetry of ten bilateral morphological traits. The participants were 40 adult male psychiatric patients and 31 adult male hospital employees. Consistent with the hypothesis, the participants' number of older brothers--but not number of older sisters, younger brothers or younger sisters--was positively associated with fluctuating asymmetry. The patients had significantly larger fluctuating asymmetry scores and tended to have more older brothers than the employees, but the positive relationship between the number of older brothers and fluctuating asymmetry was observed in both groups.     

The repeatability of fluctuating asymmetry: a revision and extension

Fluctuating asymmetry (FA) is an imperfect measure of the developmental stability of an individual. Estimates of the heritability of FA will underestimate the heritability of developmental stability; the extent of this bias can be estimated and corrected by estimating the repeatability of developmental stability. This note corrects an error in a previous derivation of this repeatability using the absolute value of the difference between sides as the measure of FA, and derives the repeatability of developmental stability for another common measure of FA, the variance among sides within an individual.     

Mixture analysis of asymmetry: modelling directional asymmetry, antisymmetry and heterogeneity in fluctuating asymmetry

The occurrence of different forms of asymmetry complicates the analysis and interpretation of patterns in asymmetry. Furthermore, between-individual heterogeneity in developmental stability (DS) and thus fluctuating asymmetry (FA), is required to find relationships between DS and other factors. Separating directional asymmetry (DA) and antisymmetry (AS) from real FA and understanding between-individual heterogeneity in FA is therefore crucial in the analysis and interpretation of patterns in asymmetry. In this paper we introduce and explore mixture analysis to (i) identify FA, DA and AS from the distribution of the signed asymmetry, and (ii) to model and quantify between-individual heterogeneity in developmental stability and FA. In addition, we expand mixtures to the estimation of the proportion of variation in the unsigned FA that can be attributed to between-individual heterogeneity in the presumed underlying developmental stability (the so-called hypothetical repeatability). Finally, we construct weighted normal probability plots to investigate the assumption of underlying normality of the different components. We specifically show that (i) model selection based on the likelihood ratio test has the potential to yield models that incorporate nearly all heterogeneity in FA; (ii) mixtures appear to be a powerful and sensitive statistical technique to identify the different forms of asymmetry; (iii) restricted measurement accuracy and the occurrence of many zero observations results in an overestimation of the hypothetical repeatability on the basis of the model parameters; and (iv) as judged from the high correlation coefficients of the normal probability plots, the underlying normality assumption appears to hold for the empirical data we analysed. In conclusion, mixtures provide a useful statistical tool to study patterns in asymmetry.     

Increased fluctuating asymmetry in the damselfly Coenagrion puella is correlated with ectoparasitic water mites: implications for fluctuating asymmetry theory

The influence of ectoparasitic water mite larvae (Arrenurus) on the fluctuating asymmetry (FA) of forewing length and cell number in the foreweings of the damselfly Coenagrion puella has been investigated. We show a significant correlation between the FA of forewing length and the mite load. Most explanations for increases in FA implicate environmental stress combined with the inability of the genome to stabilize the phenotype. In contrast, our results demonstrate that FA could be the result of a very short-term impact during ontogenesis, due to chance parasitism.     

Human fluctuating asymmetry in relation to health and quality: a meta-analysis

Developmental instability (DI) reflects the inability of a developing organism to buffer its development against random perturbations, due either to frequent, large perturbations or to a poor buffering system. The primary measure used to assess DI experienced by an individual organism is fluctuating asymmetry (FA), asymmetry of bilateral features that are, on average in a population, symmetrical. A large literature on FA in humans in relation to measures of health and quality (close to 100 studies and nearly 300 individual effect size estimates) has accumulated. This paper presents the first quantitative meta-analysis of this literature. The mean effect size (scaled as Pearson r) was about 0.2. Effect sizes covaried negatively with sample size, consistent with effects of publication bias, the tendency for significant effects to be published. Conservative correction for this bias reduced the mean effect to about 0.1. Associations with FA underestimate effects of underlying DI due to imprecise measurement of the latter. A model-based best estimate of the mean effect of DI on outcomes is about 0.3, a theoretically meaningful, relatively large effect, albeit of moderate absolute size. The data are consistent, however, with a range of true effect sizes between 0.08 and 0.67, partly due to large study effects. Study-specific effect sizes in DI ranged between −0.2 and 1.0. A humbling and perhaps sobering conclusion is that, in spite of a large body of literature involving nearly 50 000 participants, we can only confidently state that there is on average a robust positive average effect size. An accurate estimate of that effect size was not possible, and between-study variation remained largely unexplained. We detected no robust variation across six broad categories of outcomes (health and disease, fetal outcomes, psychological maladaptation, reproduction, attractiveness and hormonal effects), though examination of narrower domains reveal some corrected effects close to 0.2 and others near zero. The meta-analysis suggests fruitful directions for future research and theory.     

Morphological integration of fluctuating asymmetry in the mouse mandible

Morphological integration of fluctuating asymmetry (FA) was assessed for nine mandibular characters in random-bred house mice to test the hypothesis that there should be a significant integration or concordance of FAs at the population level, but not at the individual level. FA estimates for each of the nine characters were made for each of 16 subpopulations (two replicates each for mice varying in sex and age) and their correlations indicated a moderate level of integration (index of integration = 0.42). A matrix permutation test of the differences of the correlations within two (‘incisor’ and ‘muscle’) developmentally different character groups versus correlations between groups was significant, indicating the presence of morphological integration. Kendall's coefficient of concordance also indicated a significant population asymmetry parameter for FAs within the two character groups. Correlations among individual FA estimates were generally lower than those calculated from subpopulations, the index of integration being 0.21. The matrix permutation test failed to show significant morphological integration among individual FAs, but Kendall's coefficient of concordance was significant, indicating the presence of an ‘individual asymmetry parameter’ among the nine characters. Principal components analysis and canonical correlation analysis confirmed the overall higher level of integration of FAs among the subpopulations and within the two character groupings.     

On the meaning of increased fluctuating dental asymmetry: a cross populational study.

Suarez reports a greater magnitude of fluctuating dental asymmetry for Neandertal sample when compared with a sample of modern Ohio whites. He postulates that this greater antimeric variance could be due to a greater degree of inbreeding in the Neandertal populations. In the present investigation, the magnitude of fluctuating dental asymmetry is evaluated for Eskimo and Pueblo populations. These populations were found to exhibit dental variance of equal magnitude to that of the Neandertal population. As these populations are not highly inbred, a stress related mechanism is suggested to explain these observations and the inbreeding hypothesis is rejected. The implications of this mechanism to Brace's Probable Mutation Effect are discussed.     

'Vertition' of integumental organs in mites revisited: a case of fluctuating asymmetry.

Vertition in mites is defined as a meristic variation for a bilateral integumental organ with a separate genetic control for each body side. A prominent hypothesis expressed by Grandjean is the role of vertition in the evolutionary trend towards a reduced number of hair-like organs (mechano- and/or chemo-receptors) known to have occurred in many mite groups. Observations on leg setae in the two-spotted spider mite Tetranychus urticae do not support this hypothesis. Meristic variation for leg setae rather conforms to the notion of fluctuating asymmetry: the difference between the number of leg setae on the right and left sides of the body had a unimodal distribution with a mean of zero. Moreover, lack of heritability for left/right absences of leg setae in an inbred laboratory strain suggests that vertition could be purely environmental. It is therefore argued that meristic variation for hair-like organs in mites is caused by random developmental accidents not corrected by homeostatic mechanisms normally resulting in a perfect bilateral symmetry.     

Patterns of inter-annual variation in the size asymmetry of growth in Pinus banksiana

A large body of literature suggests that asymmetric competition, where large individuals suppress the growth of smaller individuals by intercepting a disproportionate share of incoming light, is a dominant process in tree population development. This has not been examined extensively for long-lived tree species that accumulate growth over many years under varying growing conditions. Using dendrochronological techniques, we reconstructed annual growth and mortality rates at ten stands of jack pine (Pinus banksiana Lamb.) in Western Canada. We used these data to calculate an annual index of the size asymmetry of growth for each stand for the last 50 years. Jack pine is a shade-intolerant species found in even-aged monoculture stands, so the simple hypothesis is that large trees should consistently perform relatively better than small trees. Inter-annual variation in the index of size-asymmetric growth was positively associated with interannual variation in stand productivity at eight of ten sites. The size asymmetry of growth also showed a positive trend with age at eight of ten sites, even though all sites were in a period of declining leaf area. This should have reduced the intensity of asymmetric competition for light and reduced the size asymmetry of growth over time. Alternate hypotheses for this trend are (1) that physical collisions between crowns result in asymmetric competition for growing space because they are more damaging to small trees, or (2) that a differential build up of diseases in susceptible trees suppresses their growth, even in the absence of competition.     

Interpopulation variation in fluctuating asymmetry of the palmar A-B ridge-count

Fluctuating asymmetry was measured by the Pearson correlation coefficient between a-b ridge-counts of the right and left hands. Such data were available for 38 samples, which were grouped by major geographical regions. Significant heterogeneity exists within some of the geographical groups but the between geographical group component is highly significant in both sexes. Our results show that a sizable fraction of variation in fluctuating asymmetry is related to geographical race. There is no evidence that it follows environmental or ecological lines. The variation between geographical races suggests that there is a genetic component in the magnitude of fluctuating asymmetry.     

Geography of fluctuating asymmetry in the greenfinch, Carduelis chloris

Levels of fluctuating asymmetry (FA) in 12 bilateral skeletal traits were estimated from 12 populations of greenfinches (Carduelis chloris) collected along a north‐south gradient across Europe. Average FA of measured traits was positively correlated with latitude indicating that the younger and genetically less diverse northern European populations are developmentally less stable than the older and genetically more diverse southern populations. Levels of FA differed significantly between different traits being lowest for functionally important traits (limb and wing bones) and highest for functionally less important traits such as foramina (apertures through bones)– a pattern that was highly concordant across different populations. Males tended to exhibit higher levels of FA than females, a finding consistent with the suggestions that males are more prone to developmental perturbations than females. Age differences in levels of FA were relatively clear, but inconsistent across traits with different degree of functionality. Individual heterozygosity – as enumerated from variation in allozyme loci – was unrelated to individual FA. No evidence for existence of individual asymmetry parameter (IAP) was found although traits related to locomotion indicated some degree of integration, which was expressed by correlations in the signed asymmetry. Nevertheless, an individual's overall asymmetry was poorly predicted by asymmetry of individual characters. Evidence for existence of population asymmetry parameter (PAP) was clear since all traits exhibited a similar degree of association with latitude. That the latitudinal cline of increasing FA towards north coincided with decreasing levels of genetic variability across the cline could be indicative of break down of developmental stability in the recently established and genetically impoverished populations. To what extent a reduced heterozygosity, the break up of co‐adapted gene complexes and/or environmental differences contributed to this process cannot be distinguished from our data.     

Individual differences in developmental precision and fluctuating asymmetry: a model and its implications

In many studies, fluctuating asymmetry (FA) has been used as a measure of individual differences in developmental imprecision. A model of how variation in developmental imprecision is associated with variation in asymmetry is described and applied to important issues about FA. If individual differences in developmental imprecision exist, asymmetry due to developmental error should be leptokurtically distributed. Moreover, the greater the magnitude of individual differences, the greater the leptokurtosis. Asymmetry purportedly due to developmental error in a variety of species is indeed leptokurtically distributed. The level of leptokurtosis suggests that the CV in individual differences in underlying developmental imprecision is generally 20–25, consistent with it being a fitness trait. In addition, data suggest that: (1) the individual differences that underlie the developmental imprecision of different traits are largely shared across traits and not trait-specific; (2) the heritability of these individual differences may average between 35 and 55%, despite small heritabilities of individual trait FAs; and (3) correlations between FA and fitness traits or components suggest high correlations between underlying variation in developmental precision and fitness in many species. Theoretical implications are discussed.     

High levels of fluctuating asymmetry in isolated stickleback populations

ABSTRACT: BACKGROUND: Fluctuating asymmetry (FA), defined as small random deviations from the ideal bilateral symmetry, has been hypothesized to increase in response to both genetic and environmental stress experienced by a population. We compared levels of FA in 12 bilateral meristic traits (viz. lateral-line system neuromasts and lateral plates), and heterozygosity in 23 microsatellite loci, among four marine (high piscine predation risk) and four pond (zero piscine predation risk) populations of nine-spined sticklebacks (Pungitius pungitius). RESULTS: Pond sticklebacks had on average three times higher levels of FA than marine fish and this difference was highly significant. Heterozygosity in microsatellite markers was on average two times lower in pond (HE [almost equal to] 0.3) than in marine (HE [almost equal to] 0.6) populations, and levels of FA and heterozygosity were negatively correlated across populations. However, after controlling for habitat effect on heterozygosity, levels of FA and heterozygosity were uncorrelated. CONCLUSIONS: The fact that levels of FA in traits likely to be important in the context of predator evasion were elevated in ponds compared to marine populations suggests that relaxed selection for homeostasis in ponds lacking predatory fish may be responsible for the observed habitat difference in levels of FA. This inference also aligns with the observation that the levels of genetic variability across the populations did not explain population differences in levels of FA after correcting for habitat effect. Hence, while differences in strength of selection, rather than in the degree of genetic stress could be argued to explain habitat differences in levels of FA, the hypothesis that increased FA in ponds is caused by genetic stress cannot be rejected.     

Variation in fluctuating asymmetry levels across a Robertsonian polymorphic zone of the house mouse

Fluctuating asymmetry (FA) levels were assessed within the Barcelona Robertsonian polymorphic zone of Mus musculus domesticus as a measure of developmental instability (DI). This zone is characterized by populations with a reduced diploid number (2n = 27–39) surrounded by others with standard karyotype (2n = 40). Mice were distributed into four classes according to mean diploid number at each collecting site, and differences in their FA levels were studied. Three different FA indices were calculated on interlandmark distances from two major morphogenetic units of the mandible: the teeth and muscular areas. Three kinds of analysis were performed: trait‐by‐trait, considering the two regions separately and pooling all traits. In univariate analyses few differences were detected between classes. Nevertheless, when characters were pooled, differences in FA values were found between one Robertsonian group and standard mice, and between several Robertsonian classes. Teeth area traits showed higher FA levels in Rb I mice, i.e. those geographically close to the standard populations. However, FA levels decreased in more introgressed Robertsonian groups and showed significant differences with Rb I. Muscular area traits showed lower DI levels in the Robertsonian mice, especially those with an intermediate mean diploid number (Rb II). When all traits were pooled, FA levels increased in Rb I, whilst the other Robertsonian groups showed similar, or even lower, FA values to those of the standard mice. The higher FA levels found in Rb I suggest an increase in the disruption of genetic coadaptation. Furthermore, in Rb I the presence of metacentrics is more recent than in more introgressed populations; we therefore suggest that Rb I have had less time to restore genetic coadaptation. In addition, the teeth region of the mandible seems to be more sensitive to genomic stress than the muscular region. In the light of these results we suggest that hybrids should be separated into groups and that mandible morphogenetic units be differentiated when using FA in hybrid zones to analyse DI.