Lizards from Urban Areas Are More Asymmetric: Using Fluctuating Asymmetry to Evaluate Environmental Disturbance

The increase in human activities that leads to wildlife decline and species extinction poses an urgent need for simple indicators of environmental stress in animal populations. Several studies have suggested that fluctuating asymmetry (FA) can be an easy, direct measure of developmental instability because it is associated to environmental stress and, as such, it can be a useful indicator of population disturbance. We examined three different morphological traits in urban and rural populations of the common wall lizard (Podarcis muralis) to test whether anthropogenic disturbance causes an increase in FA. Compared to rural populations, urban ones showed higher levels of FA in all analyzed traits, thus providing evidence that FA can respond to anthropogenic disturbance. However, we also found significant differences in FA among traits, where femoral pores and subdigital lamellae, traits with a functional relevance, were more stable developmentally compared to supracilliar granules which have no evident function. Unsigned FA [abs(right-left)] exhibited significant, but weak, positive correlations among traits, indicating that developmental noise does not have a uniform effect across characters and thus questioning the view of developmental stability as an organism-wide property. The degree of signed FA (right-left) was more similar between structurally associated traits, possibly as an outcome of morphological integration. In conclusion, our results demonstrate that FA can be a reliable indicator of disturbance provided that it is analyzed on multiple traits simultaneously and examined at the population level.     

Leaf fluctuating asymmetry of common plantain as an indicator of habitat quality

Abstract

Although developmental instability (DI), measured as fluctuating asymmetry (FA), is expected to be positively related to environmental stress and negatively to habitat quality, the pattern found here was the reverse. Developmental instability of leaf traits (leaf width and vein distances within a leaf) was estimated (using two indices of FA: FA₄ and σ_i ²) and compared between three populations of Plantago major L. (Plantaginaceae) from northern Serbia. Two of the populations are from chronically polluted areas (Karaburma & Zemun), while Crni Lug is from an unpolluted, natural area. Results obtained using both FA indices were the same; higher asymmetry levels in the unpolluted area than in the polluted sites, were found for both traits. Between the two polluted sites, FA values were significantly higher in Karaburma site for vein distances within a leaf. Concerning differences in FA₄ values between samples, in two cases, results are similar to those found for σ_i ² values, for vein distances within leaf. These are the first quantitative data on P. major indicating that (i) plants living in the stressful sites are more symmetrical and (ii) leaf FA for plant species with wide ecological distribution such as P. major should be considered as an ‘index of habitat quality.’     

DEVELOPMENTAL STABILITY IN LEAVES OF CLARKIA TEMBLORIENSIS (ONAGRACEAE) AS RELATED TO POPULATION OUTCROSSING RATES AND HETEROZYGOSITY

Four natural populations of Clarkia tembloriensis, whose levels of heterozygosity and rates of outcrossing were previously found to be correlated, are examined for developmental instability in their leaves. From the northern end of the species range, we compare a predominantly selfing population (t? = 0.26) with a more outcrossed population (t? = 0.84), which is genetically similar. From the southern end of the range, we compare a highly selfing population (t? = 0.03) with a more outcrossed population (t? = 0.58). We measured developmental stability in the populations using two measures of within-plant variation in leaf length as well as calculations of fluctuating asymmetry (FA) for several leaf traits. Growth-chamber experiments show that selfing populations are significantly more variable in leaf length than more outcrossed populations. Developmental instability can contribute to this difference in population-level variance. Plants from more homozygous populations tend to have greater within-plant variance over developmentally comparable nodes than plants from more heterozygous populations, but the difference is not significant. At the upper nodes of the plant, mature leaf length declines steadily with plant age, allowing for a regression of leaf length on node. On average, the plants from more homozygous populations showed higher variance about the regression (MSE) and lower R² values, suggesting that the decline in leaf length with plant age is less stable in plants from selfing populations than in plants from outcrossing populations. Fluctuating asymmetry (FA) was calculated for four traits within single leaves at up to five nodes per plant. At the early nodes of the plant where leaf arrangement is opposite, FA was also calculated for the same traits between opposite leaves at a node. Fluctuating asymmetry is significantly greater in the southern selfing population than in the neighboring outcrossed population. Northern populations do not differ in FA. Fluctuating asymmetry can vary significantly between nodes. The FA values of different leaf traits were not correlated. We show that developmental stability can be measured in plants using FA and within-plant variance. Our data suggest that large differences in breeding system are associated with differences in stability, with more inbred populations being the least stable.     

Developmental stability in flowers of Clarkia tembloriensis (Onagraceae)

Developmental instability of floral traits is examined in four populations of Clarkia tembloriensis (Onagraceae) with different natural outcrossing rates. Developmental instability is estimated using fluctuating asymmetry (FA) and within plant variance. The results are coupled with those from a previous study of leaf traits. In the first experiment, flowers were collected from the same growth chamber-grown plants that had been previously used to estimate leaf developmental stability in two C. tembloriensis populations. These populations differed in FA for only one floral trait, long filament length. After adjusting for organ size differences, we found floral FA values were about half those of leaves. These are the first quantitative data indicating that flowers are more developmentally stable than leaves. In a second experiment, greenhouse grown plants from two other C. tembloriensis populations (one highly outcrossing and one predominantly self-pollinating) did not differ significantly in floral FA or in within-plant variance of floral traits, though earlier studies of the same populations revealed significant differences in FA of leaf traits. In both experiments, FA values of different floral traits were uncorrelated. We attribute the lack of significant differences in floral stability between populations to the greater canalization of floral organs and to the magnification of measurement error that occurs when calculating FA. We also found that the shorter styles of selfers are the greatest difference in flower form between predominantly self-pollinating and predominantly outcrossing populations of C. tembloriensis.     

Artificial selection reveals heritable variation for developmental instability

Fluctuating (nondirectional) asymmetry (FA) of bilaterally paired structures on a symmetrical organism is commonly used to assay the developmental instability (DI) caused by environmental or genetic factors. Although evidence for natural selection to reduce FA has been reported, evidence that FA (and by extension DI) is heritable is weak. We report the use of artificial selection to demonstrate heritable variation in the fluctuating asymmetry of interlandmark distances within the wing in an outbred population of Drosophila melanogaster. Our estimates for the heritability of FA range from 0% to 1% and result in estimates for the heritability of DI as large as 20%, comparable to values typical for life-history traits. These values indicate the existence of evolutionarily relevant genetic variation for DI and the effectiveness of selection for reduced FA suggests that natural selection has not fixed all the genetic variants that would improve developmental stability in these populations.     

Off-Highway Vehicle Trail Impacts on Breeding Songbirds in Northeastern California

Abstract: Rapid growth in off-highway vehicle (OHV) use in North America leads to concerns about potential impacts on wildlife populations. We studied the relationship between distance to active OHV trail and songbird nesting success and abundance in northeastern California, USA, from 2002 to 2004. We found evidence of greater nest desertion and abandonment and reduced predation on shrub nests <100 m from OHV trails than at nests >100 m from OHV trails. Two of 18 species studied were less abundant at sites on trails than at sites 250 m from trails, and no species were more abundant on trails. Management of OHV trail development should consider possible negative impacts on nesting success and abundance of breeding birds.     

Developmental instability and inbreeding in natural bird populations exposed to different levels of habitat disturbance

As habitat disturbance and inbreeding increasingly stress natural populations, ecologists are in urgent need of simple estimators to measure their impact. It has been argued that developmental instability (DI) could be such a measure. Observed associations between DI and environmental or genetic stress, however, are largely inconsistent. We here test whether an interaction between habitat disturbance and inbreeding could, at least partly, explain these discordant patterns. We therefore studied individual estimates of fluctuating asymmetry (FA) and of inbreeding in three populations of the critically endangered Taita thrush that are differentially exposed to habitat disturbance following severe forest fragmentation. As predicted, the relationship between DI and inbreeding was pronounced under high levels of disturbance, but weak or nonexistent under less disturbed conditions. Examining this relationship with mean d², an allelic distance estimator assumed to reflect ancestral inbreeding, did not reveal any significant trend, hence suggesting that inbreeding effects in the Taita thrush are fairly recent.     

FLUCTUATING ASYMMETRY IN A SALIX HYBRID SYSTEM: THE IMPORTANCE OF GENETIC VERSUS ENVIRONMENTAL CAUSES

To examine the effects of hybridization and environmental stress on developmental instability, we examined fluctuating asymmetry (FA), the variance in random deviations from perfect symmetry in bilaterally symmetrical traits, for leaf symmetry in a Salix hybrid system. An abiotic environmental stress (water stress), an interspecific biotic stress (pathogen attack), and an intraspecific biotic stress (competition) were examined to determine which factors increase developmental instability. None of these three environmental stressors significantly increased FA. However, genetic stress through hybridization was detected; hybrid plants showed significantly higher levels of FA than parental species. In contrast to hybridization providing greater developmental stability through heterozygosity, these results suggest that complex, nonadditive interactions provided developmental stability and that developmental instability increased when coadapted gene complexes were disrupted through hybridization. In addition, plant biomass was significantly, negatively correlated with FA, suggesting that those individuals that were more able to buffer themselves against the disruptive effects of environmental stress may have a selective advantage over those that are less able to buffer themselves against these disruptive effects.     

GENOMIC COADAPTATION AND DEVELOPMENTAL STABILITY WITHIN INTROGRESSED POPULATIONS OF ENNEACANTHUS GLORIOSUS AND E. OBESUS (PISCES,CENTRARCHIDAE)

Using fluctuating bilateral asymmetry as a measure of developmental stability, we tested the hypothesis that genomic coadaptation mediates developmental stability in natural populations. Hybrid populations were more asymmetrical than populations of the parental species, and ranks of overall developmental instability were positively correlated with ranks of mean heterozygosity in these populations. The failure to find increased asymmetry in previous studies of natural hybrid populations (Jackson, 1973a, 1973b; Felley, 1980) suggests that such populations may have re-evolved coadapted genomes. Increased asymmetry in hybrid Enneacanthus populations may reflect the youthfulness of these populations.     

Fluctuating asymmetry in leaves and flowers of sympatric species in a tropical montane environment

Fluctuating asymmetry (FA) represents small, random variations in traits, presumably with bilateral symmetry, and is widely used as a tool to measure developmental instability in plants and animals. Because FA is a quick, simple and reliable measure, it has been frequently used for monitoring levels of environmental stress. This study investigated whether FA can be used as a predictor of individual developmental instability for four sympatric Melastomataceae species. To achieve that aim, 20 individuals of Trembleya laniflora, T. parviflora, Lavoisiera campos‐portoana and Tibouchina heteromalla were marked in southeastern Brazil and monitored before and during the flowering season. The FA index was calculated as the mean of the difference in the width or length between the left and right sides measured for each leaf or flower. All studied species exhibited asymmetry in the leaves and flowers, but the leaves of L. campos‐portoana and the petal width of T. heteromalla exhibited directional asymmetry, also an indicator of developmental instability. The highest level of leaf asymmetry was found in T. heteromalla and on flowers of L. campos‐portoana. None of the studied species exhibited a significant relationship between the FA level of the leaves and flowers on an individual basis, indicating that environmental and/or genetic sources of stress might act differently on different plant traits. For the studied species, measurements of FA can be suggested as useful tools to biomonitor levels of stress experienced by both leaves and flowers within the Melastomataceae family.     

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.     

Relationship between fluctuating asymmetry and fitness within and between stressed and unstressed populations of the wolf spider Pirata piraticus

Although developmental instability, measured as fluctuating asymmetry (FA), is expected to be positively related to stress and negatively to fitness, empirical evidence is often lacking or contradictory when patterns are compared at the population level. We demonstrate that two important properties of stressed populations may mask such relationships: (i) a stronger relationship between FA and fitness, resulting in stronger selection against low quality (i.e. developmental unstable) individuals and (ii) the evolution of adaptive responses to environmental stress. In an earlier study, we found female wolf spiders Pirata piraticus from metal exposed populations to be characterized by both reduced clutch masses and increased egg sizes, the latter indicating an adaptive response to stress. By studying the relationship between these two fitness related traits and levels of FA at individual level, we here show a significant negative correlation between FA and clutch mass in metal stressed populations but not in unstressed reference populations. As a result, levels of population FA may be biased downward under stressful conditions because of the selective removal of developmentally unstable (low quality) individuals. We further show that females that produced larger eggs in stressed populations exhibited lower individual FA levels. Such interaction between individual FA and fitness with stress may confound the effect of metal stress on FA, resulting in an absence of relationships between FA, fitness and stress at the population level.     

Developmental stability in brown trout: are there any effects of heterozygosity or environmental stress?

We studied the developmental stability of brown trout, Salmo trutta L., in 10 populations (five acidified, five control) in Norway, measured as fluctuating asymmetry (FA) and departure from the morphological norm. We measured four meristic and four morphometric characters, and scored the level of biochemical heterozygosity at 49 loci (20 polymorphic). We reared eggs of a single population in a hatchery using four different water qualities (three replicates of each treatment) to test the effect of acidification stress on developmental instability. There were no significant differences in the level of FA, in departure from the morphological norm between brown trout sampled from lakes with acidified or control water qualities, or in brown trout hatched at different water qualities. There was no correlation between level of heterozygosity and FA or departure from the morphological norm, either when tested within populations or among populations. There were no single-locus effects on developmental stability tested for 11 loci. We conclude that measures of developmental stability or morphological variability are not useful for detecting acidification stress in brown trout. Furthermore, we conclude that developmental stability in our material varies independently of heterozygosity.     

Does fluctuating asymmetry constitute a sensitive biomarker of nutritional stress in house sparrows (Passer domesticus)?

Small random deviations from left–right symmetry in bilateral traits, termed fluctuating asymmetry (FA), are theoretically predicted to increase with environmental stress and believed to constitute a potential biomarker in conservation. However, reported relationships between FA and stress are generally weak and variable among organisms, traits and stresses. Here we test if, and to what extent, FA increases with nutritional stress, estimated from independent feather growth measurements, in free-ranging house sparrows (Passer domesticus). Ptilochronological feather marks showed significant heterogeneity among study plots, indicating that house sparrow populations were exposed to variable levels of nutritional stress during development. However, individuals from more stressed populations did not show increased levels of fluctuating asymmetry in tarsus or rectrix length, nor was there evidence for significant between-trait concordance in FA at the individual or the population level. Lack of support for FA in tarsus and rectrix length as estimator of nutritional stress in house sparrows may indicate that developmental instability is insensitive to nutritional stress in this species, poorly reflected in patterns of fluctuating asymmetry due to ecological or statistical reasons, or highly context-specific. Such uncertainty continues to hamper the use of FA as a biomarker tool in conservation planning.     

Impact of sewage pollution on two species of sea urchins in the Mediterranean Sea (Cortiou,France): Radial asymmetry as a bioindicator of stress

BackgroundThe surroundings of the Cortiou sewage are among the most polluted environments of the French Mediterranean Sea (Marseilles, France). So far, no studies have precisely quantified the impact of pollution on the development of organisms in this area.MethodsWe used a fluctuating asymmetry (FA) measure of developmental instability (DI) to assess environmental stress in two species of radially symmetric sea urchins (Arbacia lixula and Paracentrotus lividus). For six sampling sites (Cortiou, Riou, Maire, East Maire, Mejean, and Niolon), levels of FA were calculated from continuous and discrete skeletal measures of ambulacral length, number of pore pairs and primary tubercles.ResultsFor both species, the most polluted sampling site, Cortiou, displayed the highest level of FA, while the Maire and East Maire sampling sites displayed the lowest levels. A. lixula revealed systematic differences in FA among sampling sites for all characters and P. lividus showed differences in FA for the number of primary tubercles.ConclusionsStatistical analyses of FA show a concordance between the spatial patterns of FA among sampling sites and the spatial distribution of sewage discharge pollutants in the Cortiou area. High developmental stress in these sampling sites is associated with exposure to high concentrations of heavy metals and many harmful organic substances contained in wastewater. FA estimated from structures with complex symmetry appears to be a fast and reliable tool to detect subtle differences in FA. Its use in biomonitoring programs for inferring anthropogenic and natural environmental stress is suggested.     

Asymmetry patterns across the distribution range: does the species matter?

An important question in evolutionary ecology is whether different populations across a species range, from core to periphery, experience different levels of stress. The estimation of developmental instability has been proposed as a useful tool for quantifying the degree of environmental and genetic stress that individuals experience during their development. Fluctuating asymmetry, the unsigned difference between the two sides of a bilaterally symmetrical trait, has been suggested to reflect the levels of developmental instability in a population. As such, it has been proposed as a useful tool for estimating changes in developmental instability and in stress response in populations across a range of environmental conditions. Recent studies focusing mostly on birds have detected increasing fluctuating asymmetry from core to periphery across the distribution range, suggesting that peripheral populations may experience higher levels of environmental and/or genetic stress. Most of these comparisons were done for single taxa across a single gradient. However, different species are predicted to respond differently to environmental shifts across the range. We compared asymmetry patterns in wing morphology in populations of two Euchloe butterfly species across their opposing ranges in Israel. Contrary to the patterns observed in birds across the same gradient, bilateral asymmetry did not increase or shift towards the periphery in either of the butterfly species. If fluctuating asymmetry in these traits reflects levels of stress, these results may partly reflect the fact that the range of these two butterfly species is limited by the distribution of their host plant, rather than by abiotic environmental variables. In addition, developing pierids can diapause during harsh seasons and can persist in resource‐rich patches, thus minimizing the environmental stress perceived by developing individuals. We conclude that accounting for differences in species’ life histories and range‐limiting factors is necessary in order to better predict patterns of developmental instability across spatial and environmental gradients. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 81 , 313–324.     

Developmental stability covaries with genome-wide and single-locus heterozygosity in house sparrows

Fluctuating asymmetry (FA), a measure of developmental instability, has been hypothesized to increase with genetic stress. Despite numerous studies providing empirical evidence for associations between FA and genome-wide properties such as multi-locus heterozygosity, support for single-locus effects remains scant. Here we test if, and to what extent, FA co-varies with single- and multilocus markers of genetic diversity in house sparrow (Passer domesticus) populations along an urban gradient. In line with theoretical expectations, FA was inversely correlated with genetic diversity estimated at genome level. However, this relationship was largely driven by variation at a single key locus. Contrary to our expectations, relationships between FA and genetic diversity were not stronger in individuals from urban populations that experience higher nutritional stress. We conclude that loss of genetic diversity adversely affects developmental stability in P. domesticus, and more generally, that the molecular basis of developmental stability may involve complex interactions between local and genome-wide effects. Further study on the relative effects of single-locus and genome-wide effects on the developmental stability of populations with different genetic properties is therefore needed.     

Fluctuating feather asymmetry in relation to corticosterone levels is sex-dependent in Eurasian treecreeper (Certhia familiaris) nestlings

Fluctuating asymmetry (FA) has been widely used as a stress-related phenotypic marker of developmental instability. However, previous studies relating FA to various stressful conditions have produced inconsistent results and we still lack quantitative individual-level evidence that high FA is related to stress in wild vertebrate species. We studied how baseline plasma levels of corticosterone predicted FA of wing and tail feathers in free-living Eurasian treecreeper (Certhia familiaris) nestlings. We found a sex-specific association between corticosterone levels and FA: high corticosterone levels were related to an increased FA in male but not in female nestlings. These results suggest that in treecreepers, FA may correlate with individual stress hormone levels, male developmental trajectory being potentially more sensitive to stress than that of the female.     

Morphological variability and developmental instability in subpopulations of the Eurasian badger (Meles meles) in Denmark

Aim Local populations from different geographical regions may differ in the selection regimes to which they are exposed. Differences in environmental factors and population density may affect the relative importance of different selective forces (e.g. natural vs. sexual selection). We suggest a direction of investigation concerned with the developmental instability of morphological traits. The goal is to disclose putative small‐scale geographical differences in the evolutionary forces, which may be hard to detect. Location Craniometrical investigations were carried out on ninety‐eight skulls and teeth of the Eurasian badger (Meles meles) collected during the period 1995–97 from three different populations in Denmark. One of these thrives at low population density, whereas the two others are characterized by high local density. Methods The skulls were investigated for developmental instability (DI) using fluctuating asymmetry (FA) as its estimator. FA was measured on canines, molars, premolar teeth and other skull and mandible traits. For the statistical analyses, we applied nonparametric permutation tests. Results Evidence was found suggesting differentiation among populations in mean degree of FA, and the FA values measured on canines were higher in the high‐density populations. FA of the canines was significantly higher in males than females, in contrast to FA of the other traits. Evidence of a negative relationship between canine size and their FA was found, whereas no significant correlations were found between the molar and premolar teeth measures and their FA. Main conclusions Our results suggest that canines could be under directional selection stemming from intrasexual competition, which may be stronger in high‐density zones. The other teeth investigated seem to be under a stabilizing regime hence their FA is mainly affected by environmental stresses. The negative relationship between canine size and FA found in males suggests the capacity of badgers to respond in an evolutionary way to environmental changes, despite the low genetic variability previously found at the molecular level.     

Zinc and cadmium accumulation in cabbage aphid (Brevicoryne brassicae) host plants and developmental instability

Developmental instability in morphological characters can occur during individual development due to various environmental stresses. Fluctuating asymmetry (FA) is often used as a measurement of developmental instability, but within-environment variation (CV_e) is also considered an indicator of developmental instability. Cabbage aphid ( Brevicoryne brassicae ) populations were reared on zinc- (Zn) or cadmium- (Cd) contaminated cabbage and radish plants. Developmental instability indicators were measured and their relations with fitness were explored. Results revealed that cabbage aphids exposed to Cd and Zn displayed considerable developmental instability, particularly fluctuating asymmetry. Differences in developmental instability between the two metals were also detected, as well as differences between the two developmental instability measurements. For almost all measured traits, FA was greater on Cd- and Zn-contaminated compared to non-contaminated host plants. In contrast, CV_e of some traits was greater on non-contaminated host plants, yet for other traits CV_e was greater on contaminated host plants. There were also non-significant inverse relationships between FA and fitness of cabbage aphid populations. Due to weak correlations between FA and different patterns of two developmental instability measurements, this study does not support the hypothesis that developmental instability is a useful bioindicator of environmental quality.