Heat stress, fluctuating asymmetry and prenatal selection in the laboratory rat

Recent studies have demonstrated that stress may increase the fluctuating asymmetry of teeth and limbs in laboratory animals. The present study investigates the effects of heat on such parameters. Pregnant laboratory rats are exposed to temperatures of 33 degrees C during gestation. Increases in fluctuating asymmetry of dental dimensions as well as bone density are found for the pups of such females when compared to unstressed controls. A general increase in limb lengths is also reported for young of heat stressed animals. Prenatal selection with differential survival is suggested as a possible explanation for differences found between the experimental and control animals.     

Perinatal stress and increased fluctuating asymmetry of dental calcium in the laboratory rat

Recent studies have consistently reported an increased magnitude of fluctuating dental, long bone, and membranous bone asymmetry as a function of perinatal stress. The present study was designed to test the hypothesis that increases in the fluctuating asymmetry of calcium may be related to the metric changes in these calcium-dependent systems. Pregnant rats were exposed to noise stress from conception through weaning. Bilateral lower first molars were extracted from the neonates, and calcium levels were determined using a standard atomic absorption technique. Levels of fluctuating asymmetry of calcium were found to be significantly increased (p less than .01) in the audiogenic noise-stressed group compared to unstressed, normal controls. These results follow the pattern reported earlier for metric analysis of the dentition and support a stress-induced calcium-transport-disruption hypothesis.     

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.     

Problems of sampling and inference in the study of fluctuating dental asymmetry

Randomly distributed or “fluctuating” dental asymmetry has been accorded evolutionary meaning and interpreted as a result of environmental stress. However, except for congenital malformation syndromes, the determinants of human crown size asymmetry are still equivocal. Both a computer simulated sampling experiment using a combined sample size of N = 3000, and the requirements of adequate statistical power show that sample sizes of several hundred are needed to detect population differences in dental asymmetry. Using the largest available sample of children with defined prenatal stresses, we are unable to find systematic increases in crown size asymmetry. Given sampling limitations and the current inability to link increased human dental asymmetry to defined prenatal stresses, we suggest that fluctuating dental asymmetry is not yet established as a useful and reliable measure of general stress in human populations.     

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.     

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.     

Confirmation bias in studies of fluctuating asymmetry

Fluctuating asymmetry (FA) represents small, non-directional deviations from perfect symmetry in morphological characters. FA is generally accepted to increase in response to stress; therefore, FA is frequently used in ecological studies as an index of stress experienced by an organism, in particular due to environmental pollution. We experimentally tested the hypothesis that the outcomes of studies based on FA measurements may have been influenced by confirmation bias, i.e. the tendency of humans to seek out evidence in a manner that confirms their hypotheses and beliefs. We collected 100 leaves of downy birch (Betula pubescens) from a single tree, grouped them haphazardly into ten samples, scanned every sample, and then asked each of 31 scientists (experienced in studying FA) to measure FA from the scanned images of all 100 leaves. Three groups of participants were provided with false information about the origin of each sample and about the hypothesis to be tested, and one group (control) was provided with true information. The participants who believed that the leaves originated from a heavily polluted site reported significantly higher values of FA when compared to the participants who believed that the leaves were collected from an unpolluted site. When the participants were told that half the samples originated from a polluted site and half from a clean site and were asked to attribute each sample to either of these sites based on leaf FA, the differences in FA between samples classified as ‘polluted’ and ‘unpolluted’ were much higher than the differences obtained from measurements of the same sets of samples made by the control group. We conclude that when scientists expected to find high FA in some samples, the results of their measurements confirmed their expectations. This effect, classified as confirmation bias, may considerably influence the outcomes of the research on FA. This confirmation bias can be avoided by using a blind method, where the person conducting measurements is not aware of the origin of samples being measured. We argue that the use of blind methods is critically important for any study addressing environmental or genetic impacts on FA.     

Effect of developmental temperature stress on fluctuating asymmetry in certain morphological traits in Drosophila ananassae

In the present study, the effect of thermal stress on the variability and fluctuating asymmetry (FA) in different morphological traits, viz., thorax length (TL), sternopleural bristle number (SBN), wing length (WL), wing-to-thorax (W/T) ratio, sex comb tooth number (SCTN) and ovariole number (ON), was investigated in 10 isofemale lines of Drosophila ananassae. The phenotypic and genetic variability is higher in the flies reared at low (20 °C) and at high (30 °C) temperatures as compared to that of standard (25 °C) temperature. Further, the levels of FA of measured traits differed significantly among the three temperature regimes except SBN and SCTN in males and SBN and W/T ratio in females. Moreover, the magnitude of positional fluctuating asymmetry is similar in males reared at three different developmental temperatures for SBN and SCTN but it varies significantly for SBN in females. However, when FA across all the traits was combined into a composite index (CFA), significant differences were found for both temperature regimes and sexes. Males showed higher CFA at 30 °C whereas in females it was higher at 20 °C. The results suggest that temperature increases the levels of variability and FA but the effect seems to be trait and sex specific in D. ananassae.     

Parasites differentially increase the degree of fluctuating asymmetry in secondary sexual characters

The degree of fluctuating asymmetry has been demonstrated to reflect the ability of individuals to cope with different kinds of environmental stress (Parsons 1990). Parasites and diseases are one kind of environmental stress which most individuals encounter during their lifetime. Parasites have also been suggested to play an important role in sexual selection and the development of ornaments, since the full expression of ornaments may reflect the ability of hosts to cope with the debilitating effects of parasites. Here I report for the first time that a parasite, the haematophagous tropical fowl mite Ornithonyssus bursa (Macronyssidae, Gamasida), directly affects the degree of fluctuating asymmetry in a secondary sexual character of its host, the elongated tail of the swallow Hirundo rustica (Aves: Hirundinidae). I experimentally manipulated the mite load of swallow nests during one season by either increasing or reducing the number of mites, or keeping nests as controls. The degree of fluctuating asymmetry was measured in the subsequent year after the swallows had grown new tail ornaments under the altered parasite regime. The degree of fluctuating asymmetry was larger at increasing levels of parasites for male tail length, but not for the length of the shortest tail feather or wing length or for tail and wing length in females. These results suggest that the degree of fluctuating asymmetry in tail ornaments, but not in other feather traits, reliably reveals the level of parasite infestation. This has important implications for the ability of conspecifics to use the size and the expression of ornaments in assessment of phenotypic quality and thus in sexual selection.     

Fluctuating asymmetry in fetuses of diabetic rhesus macaques

This study examines dental fluctuating asymmetry (FA) in two samples of fetal rhesus monkeys, one composed of 19 fetuses from diabetic mothers (FDM) and the other of 20 fetuses from nondiabetic mothers. Seventeen measurements were taken on the deciduous dentition of right and left mandibles. The degree of FA was assessed by comparing FDM to fetuses of normal mothers by correlation between right and left sides, and analysis of variation differences between right and left sides. Significant FA was found for three traits based on the correlation between right and left sides and for seven traits by the between-treatment ratio of variance between sides. Distal teeth, both within and outside of a morphologic field, exhibit significantly greater FA than mesial teeth. Our results support the hypothesis that developmental instability is detectable by dental FA.     

Ecological stress memory: Evidence in two out of seven species through the examination of the relationship between leaf fluctuating asymmetry and photosynthesis

Increased morphological fluctuating asymmetry is considered as an indication that the extent of a natural stress has surpassed the ability of the genotype to maintain the normal symmetry in the body plan. Young leaves can suffer by a variety of stresses, such as nutrient deficiencies, drought, heat and cold in combination with high light. Therefore, increased morphological fluctuating asymmetry in mature leaves may be considered as an ecological indicator of such environmental pressures. Hence, deviations from symmetry in a mature leaf may be a reminder of an adversity having occurred when the leaf was young and developing. We argued that a past stress may stigmatize future photosynthesis and we searched for correlations between leaf fluctuating asymmetry and photosynthetic parameters obtained from fast chlorophyll a fluorescence rise curves in mature leaves from seven tree species. The results were species-specific, with four species (Arbutus unedo, Cercis siliquastrum, Platanus orientalis and Populus alba) showing both maximum quantum yield of photosystem II and photosynthetic performance index (PI_total sensu Strasser) to be independent of the alleged juvenile stress, while in one species (Ceratonia siliqua) the two parameters were negatively correlated to leaf fluctuating asymmetry. Interestingly, in two species (Olea europaea and Pistacia lentiscus), higher leaf asymmetry was linked with lower risk of chronic photoinhibitory damage and higher photosynthetic capacity. An ‘ecological stress memory’ may be inferred for some species improving their tolerance to future adversities and global change.     

The interaction of stressors in the induction of increased levels of fluctuating asymmetry in the laboratory rat.

Recent studies on fluctuating dental asymmetry have isolated single stressors as causative agents. Since most stressors are composite in nature, the present study was designed to determine the effects of the interaction of stressors in the induction of fluctuating dental asymmetry. Pregnant rats were assigned to one of six treatment groups and stressed with various combinations of heat, cold, noise and protein deprivation. The levels of fluctuating dental asymmetry were assessed and it was found that all protocols produced higher levels of asymmetry than found for control animals. Noise and reduced protein exhibited an additive effect and the interaction of stressors produced a reduction in litter size. Suggestions were offered for further research in this expanding field.     

Relationship between exposure to an insecticide and fluctuating asymmetry in a damselfly (Odonata,Coenagriidae)

In this study, we explored the effects of pesticide on fluctuating asymmetry (FA) levels and mortality of Ceriagrion sp. larvae. The results showed that the mortality of larval damselflies treated with pesticide was significantly higher than that treated with tap water which had been aerated for 48 h, but there were no significant differences among mortality of larvae treated with different concentrations of pesticide. Meanwhile, we found that the level of FA of the first tibia length, one of the seven bilaterally symmetrical traits (First femur length, First tibia length, Second femur length, Second tibia length, Third femur length, Third tibia length and Prementum width), differed significantly with different treatments, whereas the others did not show any significant differences. The Bonferroni (Dunn) t Tests revealed that FA of the first tibia length at 15 × 10⁻⁹ mgl⁻¹ was significantly higher than that at 1.5 × 10⁻⁹ mgl⁻¹ and control. There was no significant relationship between trait size and the absolute difference between their right and left sides. There was also no significant relationship between body size and the absolute difference between right and left sides. Trait size was significantly positively correlated with body size. FA was not associated with mortality. Therefore, we concluded that FA of the first tibia length of Ceriagrion sp. larvae may be induced by sublethal doses of pesticides. That is to say, its FA may be regarded as an indicator of reflecting the level of pesticide stress. Handling editor: K. Martens     

Covariation of fluctuating asymmetry, herbivory and chemistry during birch leaf expansion

Fluctuating asymmetry (FA) is used to describe developmental instability in bilateral structures. In trees, high FA of leaves has been assumed to indicate the level of environmental or genetic stress, and for herbivores leaves from such trees have been shown to be in some cases (though not invariably) of higher quality compared to trees with symmetrical leaves. We demonstrated that FA of birch leaves correlated positively with growth rate of leaves, and with the amount of leaf biomass consumed by larvae of the geometrid Epirrita autumnata. Since asymmetry per se cannot define leaf quality for a herbivore, we determined the biochemical compounds which covary with the degree of foliage FA, in order to elucidate relationships between leaf FA, chemistry and herbivory. High foliar FA was characteristic of birches with high initial concentrations, and rapid seasonal decline in the concentrations of gallic acid and hydrolysable tannins, and with rapid seasonal changes in the concentrations of flavonoid-glycosides and sugars. In contrast, leaf FA was not related to concentrations of proanthocyanidins, protein-bound amino acids or soluble phenylalanine, the precursor of proanthocyanidins and proteins with aromatic amino acids. The positive correlation between leaf FA and consumption by E. autumnata was presumably related to the previously demonstrated compensatory consumption of E. autumnata to high concentrations of foliar gallotannins. Furthermore, sugars are well-known feeding stimulants. We propose that the variable results in studies correlating leaf FA and herbivory may stem from variable chemical associations of FA in different plants and of species-specific effects of compounds on insects. Received: 15 July 1999 / Accepted: 24 September 1999     

Association between vent pecking and fluctuating asymmetry, heterophil to lymphocyte ratio, and tonic immobility duration in chickens

The purpose of the present study was to analyze the relationship between incidence of vent pecking, fluctuating asymmetry, heterophil to lymphocyte ratio, and tonic immobility duration in chickens. The experiment (140 birds in three different replicates) measured the fluctuating asymmetry of several traits (middle toe length, leg length, wing length, wattle length, and leg width), the heterophil to lymphocyte ratio, and the tonic immobility duration in 20-week-old pullets of five Spanish breeds of chickens (Blue Andaluza, Quail Castellana, White-faced Spanish, Red-barred Vasca, and Birchen Leonesa), and a White Leghorn population, with and without evidence of suffering from vent pecking. The number of birds per breed was 20, 24, 12, 20, 18, and 46, respectively. There was a significant difference between vent pecked and non-vent pecked birds on the relative fluctuating asymmetry of middle toe length (P < 0.05), the relative fluctuating asymmetry of birds who suffered from vent pecking being larger. The combined relative fluctuating asymmetry of the five traits approached levels of statistical significance (P = 0.08). There was a significant difference (P < 0.001) in heterophil to lymphocyte ratio and tonic immobility duration between vent pecked and non-vent pecked birds, the ratio being higher and the duration being longer in the group of birds that suffered from vent pecking. Thus, vent pecked birds were more asymmetrical, stressed and fearful than non-vent pecked birds, having increased relative fluctuating asymmetry, heterophil to lymphocyte ratio and tonic immobility duration. Differences were consistent across the breeds. Results indicate that vent pecking is associated with other measures of stress e.g. fluctuating asymmetry, heterophil to lymphocyte ratio, and tonic immobility duration.     

The influence of differential survival on the distribution of fluctuating asymmetry--a modelling approach

Fluctuating asymmetry (FA) is frequently used as a potential marker of developmental stress. It is usually assumed that the distribution of FA within a population is statistically normal with a mean of zero. The relationships between three different FA-dependent survival functions and the resultant FA distribution of surviving individuals are explored. It is shown that with any biologically plausible relationship between survival and FA the resultant distribution is not normal and that this non-normality is dependent upon the form of the survival-FA relationship. Two survival probability functions resulted in leptokurtic distributions, whereas a third generated a slight decline in kurtosis values.     

Fluctuating asymmetry of leaves is a poor indicator of environmental stress and genetic stress by inbreeding in Silene vulgaris

Fluctuating asymmetry (FA) is often used as a measure of developmental instability and has been proposed as an indicator of both environmental and genetic stress. However, the empirical evidence for the effects of stress on FA in plants is inconsistent, and there are few controlled experimental studies. We analyzed different distance- and shape-based measures of the fluctuating asymmetry of the leaves of clonally replicated self- and cross-pollinated lineages of Silene vulgaris (Moench) Garcke (Caryophyllaceae) grown under a control and seven different stress treatments (drought, copper, simulated herbivory, and two levels of nutrient deficiency and of shade). Overall, FA differed among stress treatments, but was not generally higher under stress and even reduced in some treatments. Different measures of FA were only weakly correlated. Inbreeding increased only one measure of leaf FA, and only under high stress intensities. Our findings suggest that in S. vulgaris leaf fluctuating asymmetry does not serve as an indicator of environmental stress or of genetic stress by inbreeding.     

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.