Levels Of Fluctuating Asymmetry Research Articles

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.

THE ASSOCIATION BETWEEN FLUCTUATING ASYMMETRY, TRAIT VARIABILITY, TRAIT HERITABILITY, AND STRESS: A MULTIPLY REPLICATED EXPERIMENT ON COMBINED STRESSES IN DROSOPHILA MELANOGASTER.

A number of hypotheses have been proposed about the association between developmental stability phenotypic variability, heritability, and environmental stress. Stress is often considered to increase both the asymmetry and phenotypic variability of bilateral traits, although this may depend on trait heritability. Empirical studies of such associations often yield inconsistent results. This may reflect the diversity of traits and conditions used or a low repeatability of any associations. To test for repeatable associations between these variables, multiply replicated experiments were undertaken on Drosophila melanogaster using a combination stress at the egg, larval and adult stages of reduced protein, ethanol in the medium, and a cold shock. Both metric and meristic traits were measured and levels of heritable variation for each trait estimated by maximum likelihood and parent-offspring regression over three generations. Trait means were reduced by stress, whereas among-individual variation increased Fluctuating asymmetry (FA) was increased by stress in some cases, but few comparisons were significant. Only one trait orbital bristle, showed consistent increases in FA. Changes in trait means, trait phenotypic variability, and developmental stability as a result of stress were not correlated. Extreme phenotypes tended to have higher levels of FA but only the results for orbital bristles were significant. All traits had low to intermediate heritabilities except orbital bristle, which showed no heritable variation. Only traits with low heritability and high levels of phenotypic variability may show consistent increases in FA under stress. Overall, the independence of phenotypic variability, plasticity, and the developmental stability of traits extend to changes in these measures under stressful conditions.

Developmental stability and adaptive radiation in the Spalax ehrenbergi superspecies in the Near-East

Abstract Chromosomal species of the mole rat, Spalax ehrenbergi, in Israel have been shown to display distinct adaptive strategies to increasing aridity. This adaptive radiation appeared to be associated with an increase in allozymic heterozygosity. In the present study, the developmental stability (DS) estimated by fluctuating asymmetry (FA) of dental traits was used to assess the suitability of habitat and the efficiency of adaptation to local environmental conditions among populations and chromosomal species. Although FA levels were highly heterogeneous among populations, they were not found to differ between species. DS of populations appeared, however, to be impaired at higher altitudes and in indurate soils. Since these environmental features were largely covariant, the effect of each one could not be precisely determined. Interestingly, while aridity is considered as the major selective force acting on populations southwards, DS was not altered under arid conditions, suggesting that mole rat populations were adapted to their local conditions of aridity. However, the cline of aridity is matched to several environmental and genetic clines among which are the increasing heterozygosity and recombination rate among species southwards. In studies of natural populations, the potential complementary effects of environmental and genetics on DS have to be considered and hamper the interpretation of habitat suitability expressed by DS in terms of adaptive strategies.

Variation in morphological traits and trait asymmetry in field Drosophila serrata from marginal populations

Abstract Drosophila serrata occurs along the eastern coast of Australia with a southern range boundary near Sydney. To compare levels of phenotypic variation in marginal and central populations, we examined morphological variation in populations of this species from the southern range boundary and two more northerly populations. The populations differed for wing traits and there was an increase in wing size in the marginal locations which persisted under laboratory culture. The means of wing and bristle traits increased under laboratory culture, whereas wing trait coefficients of variation and variances decreased. Heritability estimates for wing size traits tended to be lower in the field compared with the laboratory, whereas bristle and crossvein length heritabilities were similar across environments. There was evidence for heritable variation in wing and bristle traits in both the marginal and more northern populations, suggesting that genetic variation was not limiting in marginal populations. Fluctuating asymmetry (FA) was also assessed as a measure of genomic and environmental stress. There were no consistent differences among populations for the FA of individual traits, or for a total FA score summed across traits. FA levels in field parents and laboratory-reared progeny were similar. Overall, the results do not support the conjecture that levels of phenotypic and genetic variability differ between central and marginal D. serrata populations.

An analysis of temperature-induced Fluctuating Asymmetry in Asellus aquaticus (Linn.)

This study examines Fluctuating Asymmetry (FA) in the isopod Crustacean Asellus aquaticus (Linn.). FA occurs in bilaterally symmetrical traits not closely related to survival or fecundity and is the presence of small random deviations from perfect symmetry caused by environmental or genetic stress. These stresses perturb the developmental programme of the organism involved, resulting in asymmetry. FA was induced in the laboratory with temperature stress. Increasing levels of FA were found with increasing environmental temperature, but alteration between extremes of temperature was not found to be as stressful as simple increases in temperature. Extreme temperatures are, therefore, inferred to be an environmental stress for A. aquaticus.

The statistical analysis of fluctuating asymmetry: REML estimation of a mixed regression model

Abstract The unbiased estimation of fluctuating asymmetry (FA) requires independent repeated measurements on both sides. The statistical analysis of such data is currently performed by a two-way mixed ANOVA analysis. Although this approach produces unbiased estimates of FA, many studies do not utilize this method. This may be attributed in part to the fact that the complete analysis of FA is very cumbersome and cannot be performed automatically with standard statistical software. Therefore, further elaboration of the statistical tools to analyse FA should focus on the usefulness of the method, in order for the correct statistical approaches to be applied more regularly. In this paper we propose a mixed regression model with restricted maximum likelihood (REML) parameter estimation to model FA. This routine yields exactly the same estimates of FA as the two-way mixed ANOVA. Yet the advantages of this approach are that it allows (a) testing the statistical significance of FA, (b) modelling and testing heterogeneity in both FA and measurement error (ME) among samples, (c) testing for nonzero directional asymmetry and (d) obtaining unbiased estimates of individual FA levels. The switch from a mixed two-way ANOVA to a mixed regression model was made to avoid overparametrization. Two simulation studies are presented. The first shows that a previously proposed method to test the significance of FA is incorrect, contrary to our mixed regression approach. In the second simulation study we show that a traditionally applied measure of individual FA [abs(left – right)] is biased by ME. The proposed mixed regression method, however, produces unbiased estimates of individual FA after modelling heterogeneity in ME. The applicability of this method is illustrated with two analyses.

Fluctuating asymmetry inSemibalanus balanoides(Crustacea: Cirripedia) at different heights on the shore

Population level studies of fluctuating asymmetry (FA) need to incorporate clinal variation in FA for proper sampling methodologies to be employed to ensure appropriate comparisons between populations are made. FA of adult acorn barnacles.Semibalanus balanoides, in the intertidal zone offers an excellent model system for looking for such variation. This study looked at the magnitude of FA ofS. balanoidesat each of three vertical heights in the barnacle zone, in two sites on the Isle of Mull, Scotland. Unsigned FA of width of sutures between tergal and scutal plates, after correcting for size and numbers of others touched, showed significant variation across the upper, mid and lower barnacle zone. Specifically, this was a U‐shaped pattern, with individuals in the mid‐Zone being more symmetrical than those at the two extremes. It is proposed that high levels of FA in the upper zone are due to exposure stresses, while biotic factors such as competition impose developmental stress in the lower zone.

Fluctuating asymmetry, call structure and the risk of attack from phonotactic parasitoids in the bushcricket Sciarasaga quadrata (Orthoptera: Tettigoniidae).

The acoustically orienting parasitoid Homotrixa alleni (Diptera: Tachinidae) is a significant mortality factor of calling male Sciarasaga quadrata (Orthoptera: Tettigoniidae), with less than 10% of males escaping parasitism within the duration of the calling season. This study examined fluctuating asymmetry (FA) (small, random deviations from perfect symmetry) in five morphological traits in S. quadrata and its relation to the survival of calling males in the field. A significant relationship was demonstrated in only a single trait; across three consecutive field seasons and among each of the collections per season, parasitised males were shown to have significantly more asymmetric hind tibia than unparasitised males. Since the morphological development of males is complete prior to parasitoid attack, this relationship is not caused by the activities of the parasitoid. Further experimentation revealed that there was no relationship between the level of FA in the hind tibia and the success of parasitism, with males artificially parasitised in the laboratory showing no difference in FA from those where parasitism was unsuccessful. Instead, FA was shown to be negatively related to chirp length, an aspect of call structure that significantly affects the survival of calling males under parasitism risk in the field. We explore the possible reasons why more asymmetric males produce calls of shorter chirp length and hypothesise that the difference in hind tibia asymmetry seen between parasitised and unparasitised males in the field is related to host location in H. alleni rather than the inability of S. quadrata to defend itself against parasitoid attack.

Developmental instability in grayling ( Thymallus thymallus) exposed to methylmercury during embryogenesis

Embryos of grayling, Thymallus thymallus, were exposed to water with different concentrations of methylmercury (0, 0.16, 0.8, 4.0, 20 μg Hg liter −1) during egg development. After hatching they were reared in control water for 3 years. The exposure resulted in body concentrations in the newly hatched fry of 0.01, 0.09, 0.27, 0.63 and 3.80 mg Hg kg −1 wet wt, respectively. In this paper we test if there is an effect of the level of methylmercury exposure on developmental stability. We did this by measuring both the level of fluctuating asymmetry (FA) and the departure from the population's morphological norm (i.e. a measure of morphological variability). There was no effect of contamination level on FA, whereas there was a slight increase in departure from the morphological norm in the more contaminated groups. This indicates that the level of FA or the departure from some morphological norm may be uncertain estimators of the level of sub-lethal stress.

Asymmetry of Early Paleozoic trilobites

Asymmetry in fossils can arise through a variety of biological and geological mechanisms. If geological sources of asymmetry can be minimized or factored out, it might be possible to assess biological sources of asymmetry. Fluctuating asymmetry (FA), a general measure of developmental precision, is documented for nine species of lower Paleozoic trilobites. Taphonomic analyses suggest that the populations studied for each taxon span relatively short time intervals that are approximately equal in duration. Tectonic deformation may have affected the specimens studied, since deviations from normal distributions are common. Several measures of FA were applied to 3–5 homologous measures in each taxon. Measurement error was assessed by the analysis of variance (ANOVA) for repeated measurements of individual specimens and by analysis of the statistical moments of the distributions of asymmetry measures. Measurement error was significantly smaller than the difference between measures taken on each side of a specimen. However, the distribution of differences between sides often deviated from a mean of zero, or was skewed or kurtosic. Regression of levels of FA against geologic age revealed no statistically significant changes in levels of asymmetry through time. Geological and taphonomic effects make it difficult to identify asymmetry due to biological factors. Although fluctuating asymmetry is a function of both intrinsic and extrinsic factors, the results suggest that early Cambrian trilobites possessed genetic or developmental mechanisms used to maintain developmental stability comparable to those of younger trilobites. Although the measures are biased by time averaging and deviations from the normal distribution, these data do not lend strong support to ‘genomic’ hypotheses that have been suggested to control the tempo of the Cambrian radiation.

The Effects of Carbaryl Exposure of the Penultimate Larval Instars of Xathocnemis Zealandica on Emergence and Fluctuating Asymmetry

The occurrence of pesticide residues in freshwater systems has become a concern in recent decades. In order to establish biomonitoring programs it is vital to investigate the response of organisms to varying concentrations of pesticides. Levels of pollutants fluctuate in freshwater systems and thus only some instars of aquatic insects may be exposed to pollution stress. Therefore it is important to investigate the effects of exposing selected instars of potential bioindicator species. In a laboratory experiment damselfly larvae of the penultimate instar were exposed to three concentrations of carbaryl (100 ppb, 10 ppb, 1 ppb) plus controls until the adult damselflies emerged. Carbaryl at 100 ppb reduced emergence by more than 90%. The lower carbaryl concentrations did not affect emergence success but increased the developmental speed slightly. The adult damselflies from the highest concentration which did not affect emergence success (10 ppb) were analyzed for their level of fluctuating asymmetry (FA), deviation from bilateral symmetry, and compared with those from controls. The level of FA in cell patterns in wings was increased whereas the level of FA for wing length did not show any differences.

Fluctuating asymmetry in Perch, Perca fluviatilis (Percidae) from three lakes of the Region Umbria (Italy) as a tool to demonstrate the impact of man‐made lakes on developmental stability

Fluctuating asymmetry (FA), the random deviation from perfect bilateral symmetry, is the basis of an acknowledged method to analyse developmental stability in animals and plants. This study investigates the fluctuating asymmetry in perch (Perca fluviatilis L.) from one natural lake (Trasimeno) and two regulated lakes (Corbara, Piediluco) of central Italy. Seven morphometric (pectoral and ventral fins length, pre‐pectoral fin distance, pre‐ventral fin distance, pectoral‐ventral fins distance, postorbital distance, head length) and six meristic (lateral line scales, pectoral and ventral fins rays, mandibular pores, upper and lower gill rakers) bilateral characters were selected to detect fluctuating asymmetry. Total and standard length, weight, sex and age were employed to investigate growth of perch. On the basis of FA levels a comparison of the three lakes was then made. Statistical analysis shows a relationship between fluctuating asymmetry levels and growth, and the possibility to order the lakes according to FA levels. Therefore, FA can be considered a tool to detect stress occurring during development.

Dynamics of developmental stability of seals and pollution in the Baltic Sea

Zakharov V. M., Valetsky A. V. and Yablokov A. V. 1997. Dynamics of developmental stability of seals and pollution in the Baltic Sea. [In: Developmental homeostasis in natural populations of mammals: phenetic approach. V. M. Zakharov and A. V. Yablokov, eds]. Acta Theriologica, Suppl. 4: 9-16. Fluctuating asymmetry of skull characters, as a measure of developmental sta­ bility, was studied in two seal species: grey seal Halichoerus grypus (Fabricius, 1791), and ringed seal Pusa hispida Schreber, 1775 from the Baltic Sea. Seals were collected in three different periods of water pollution of the Baltic Sea. We revealed the same temporal dynamics of fluctuating asymmetry level for both species: it proved to be low in “pre-pollution period” (years 1877-1936), high for the “high-pollution period” (1964-1975), and was again low for the “low-pollution period” (1986-1990). These data suggest that changes in the condition of the seal populations in the Baltic Sea revealed by changes in developmental stability are correlated with the dynamics of the pollution level. N. K. Koltzov Institute of Developmental Biology Russian Academy of Sciences, Vavilov Str. 26, Moscow, 117808 Russia

DEVELOPMENTAL STABILITY, FITNESS, AND TRAIT SIZE IN LABORATORY HYBRIDS BETWEEN EUROPEAN SUBSPECIES OF THE HOUSE MOUSE.

The effects of hybridization on developmental stability and size of tooth characters were investigated in intersubspecific crosses between random-bred wild strains of the house mouse (Mus musculus domesticus and M. m. musculus). Fluctuating asymmetry (FA) and trait size were compared within and between parental, F1 , backcross, and F2 hybrid groups. The relationship between FA and reproductive fitness within the F1 hybrids was also studied. The results indicated that both FA and character size levels differed significantly between the two subspecies. The F1 hybrids and the recombined groups (backcrosses and F2 hybrids) showed heterosis for both parameters. No significant differences in the FA of fertile and sterile F1 hybrid individuals were found. Comparison of the FA levels obtained in this study with those found in wild populations from the hybrid zone in Denmark showed that the levels of FA were lower in laboratory-bred samples than in the wild populations. This study provides further evidence that, in hybrids, the developmental processes underlying most of the morphological traits we studied benefit from a heterotic effect, despite the genomic incompatibilities between the two European house mice revealed by previous genetical and parasitological studies.

Fluctuating Asymmetry and Body Size as Indicators of Stress in Red Squirrel Populations in Woodland Fragments

1. In large parts of Europe, red squirrels (Sciurus vulgaris) live in fragmented woodlands, where populations are small, and dispersal rate and genetic diversity are reduced. These small populations are, therefore, likely to have been exposed to substantial environmental and/or genetic stress. Fluctuating asymmetry (FA) represents a measure of the sensitivity of development to stress. 2. We examined the expression of FA in the hind foot (a non-sexually selected trait) of live-caught squirrels from two large and six small populations, of which we had data on population density, reproductive rate and genetic variation. 3. Red squirrels in woodland fragments were smaller and had a slightly higher degree of FA than squirrels from large forests. In fragments, heavier squirrels tended to have lower degrees of FA and reproducing females were less asymmetric than non-reproducers. Both relationships indicate that, in small populations, FA increased in poor quality individuals. 4. Interpopulation variation in the mean level of FA, however, could not be correlated with genetic similarity or with woodland quality. We conclude that FA in the hind foot of red squirrels is too variable to be a useful indicator of stress differences between populations.

Comment: Fluctuating asymmetry and sexual size dimorphism

Fluctuating asymmetry (FA) is defined as a small random deviation from otherwise perfect bilaterally symmetrical traits (Van Valen 1962; Palmer and Strobeck 1986). Bortolotti and Gabrielson (1995) presented two hypotheses as to why the degree of FA should vary between, the sexes of the American kestrel (Falco spawerius). First, as female kestrels are larger than males (Snyder and Wiley 1976), they require more food to grow. Assuming that parents are under food limitation, females should receive inadequate food to grow and thus should show higher levels of FA than males. Second, because of their large size, females may be dominant over males, and thus may be able to monopolize food. In this situation, males should receive inadequate food and thus should exhibit higher levels of FA than females. Bortolotti and Gabrielson did not find support for either hypothesis, as the degrees of FA did not differ significantly between the sexes. For evaluating their hypotheses, Bortolotti and Gabrielson obtained and measured kestrel skeletons from different Canadian museums. They obtained rather small samples from seven general locations (n I 3, except n I 25 for Ontario and Alberta, and five specimens from unknown locations). The fact that specimens were obtained from populations with unknown histories, coupled with a wrong assumption about the lack of a genetic basis for FA, has made Bortolotti and Gabrielson's analysis hard to interpret. Bortolotti and Gabrielson (1995, p. 141) stated that FA is almost entirely caused by environmental stress and that genetic differences among subjects have no effect on such a phenomenon. Three types of genetic stress can affect FA: loss of heterozygosity, hybridization, and an influx of new mutants through natural selection (Leary and Allendorf 1989). There is evidence for all these three genetic processes affecting FA (e.g., Soul6 1979; Leamy 1984; Leary et al. 1984). Although there is some debate regarding the genetic basis of FA, it cannot be fully excluded (Clarke 1994, 1995). Therefore, Bortolotti and Gabrielson cannot rule out genetic differences among the populations from which their speci-

Habitat structure, stress and plumage development

Past studies have demonstrated that birds’ perceived risk of predation is influenced by habitat structure, notably the availability of a refuge and the location of food. Thus apparently dangerous habitats, such as those without a refuge, may act as stressors to birds. We test the hypothesis that habitat structure influences stress by manipulating cover availability and food location in European starlings, Sturnus vulgaris , housed in large flight aviaries during moult. We use degree of fluctuating asymmetry (FA) and the number of fault bars in primary feathers to measure stress. The manipulations had no effect on the overall timing or rate of moult, or on the final size and shape of the wings. However, birds from aviaries with cover had lower levels of FA and fewer faults than birds from aviaries without cover. Food location also influenced FA, with birds from aviaries with food located near to cover having lower levels of asymmetry; however, this effect was weak and transitory, only influencing the first primary growth during moult. Food location did not influence the number of fault bars. These results indicate that manipulations of habitat structure can influence stress. Although plumage development may be influenced by perceived risk of predation per se, the possible role of other proximate determinants of plumage abnormalities such as changes in feeding patterns, activity levels, and incidence of mechanical damage are also considered.

Chest plumage, dominance and fluctuating asymmetry in female starlings

It has been proposed that levels of fluctuating asymmetry (FA) may be used in establishing and maintaining dominance hierarchies, as asymmetry reflects aspects of individual quality. However, previous manipulations of FA have failed to reveal that the level or outcome of agonistic intra-sexual interactions are affected by levels of FA. In female European starlings (Sturnus vulgaris), correlational data suggest that FA of the speckled chest plumage may be related to dominance status. These data are confounded, however, by total number of spots on the chest and the proportion of the chest that is white, both of which positively covary with chest asymmetry. Thus, we deconfounded the effects of these plumage traits on dominance by experimentally manipulating the number of spots and spot number asymmetry in a factorial design. The results indicated that dominance is influenced by the number of spots on the chest, but not by spot asymmetry. Birds with spottier chests were dominant over birds with experimentally decreased spot number. We suggest that female starlings' chests are exposed to extensive abrasion throughout the breeding season and so are susceptible to damage asymmetries that may mask the `true' fluctuating asymmetry of the trait. This may devalue the use of chest asymmetry as a quality indicator. Spottier chests may be costly to maintain, in part because of increased susceptibility to abrasion, and so may be a better indicator of quality than asymmetry.

Female preference for symmetrical males as a by-product of selection for mate recognition.

Fluctuating asymmetry (FA) refers to the random, stress-induced deviations from perfect symmetry that develop during the growth of bilaterally symmetrical traits. Individual differences in the level of FA may influence mate choice: in a number of species, females prefer to mate with males that have more symmetrical sexual ornaments. As the degree of FA has been shown to reflect the ability of individuals to cope with a wide variety of environmental stresses, it has been suggested that mating preferences for symmetry evolve for adaptive reasons, because the degree of FA provides honest information about male quality. Here I use simple, artificial neural networks to show that such preferences are likely to arise in the absence of any link between symmetry and quality, as a by-product of selection for mate recognition.

Fluctuating asymmetries, competition and dominance

Levels of fluctuating asymmetry (FA) in the primary feathers of European starlings, Sturnus vulgaris, have been shown to be sensitive to nutritional and energetic stress. Furthermore, between-individual variation in plumage FA has been found to be related to social dominance, even without social interactions during feather growth, with dominant birds exhibiting the highest levels of FA. Here we examine whether the relation between dominance and FA differs when birds are housed in social groups, under different degrees of competition for food, during moult. We reason that dominants should derive a greater benefit from their social status as competition for food increases. Our results support this proposition. The relation between dominance and FA differed significantly according to the degree of competition for food. However, in no cases did the dominants exhibit lower levels of FA than subdominants. When competition for food was low, dominants had higher levels of FA than subdominants. When competition for food was high, there was no systematic relation between dominance and FA. These results suggest that dominants may only derive a net benefit from their social status, under the circumstances of our experiment, during severe conditions of competition.