GENETICS OF FLUCTUATING ASYMMETRY: A DEVELOPMENTAL MODEL OF DEVELOPMENTAL INSTABILITY

Although numerous studies have found that fluctuating asymmetry (FA) can have a heritable component, the genetic and developmental basis of FA is poorly understood. We used a developmental model of a trait, according to a diffusion-threshold process, whose parameters are under genetic control. We added a small amount of random variation to the parameter values of this model to simulate developmental noise. As a result of the nonlinearity of the model, different genotypes differed in their sensitivity to developmental noise, even though the noise is completely random and independent of the genotype. The heritable component of FA can thus be understood as genetically modulated expression of variation that is itself entirely nongenetic. The loci responsible for this genetic variation of FA are the same that affect the left/right mean of the trait, showing that genetic variation for FA does not require genes that specifically control FA. Furthermore, the model offers alternative explanations for phenomena widely discussed in the literature on FA, for instance, the correlations between FA and heterozygosity and between FA and trait size. The model underscores the importance of dominance and epistasis, and therefore unites the study of FA with the classical theory of quantitative genetics.     

ESTIMATING THE HERITABILITY OF FLUCTUATING ASYMMETRY IN FIELD DROSOPHILA

Some studies have found intermediate heritabilities for fluctuating asymmetry (FA) in traits, but almost all of these are flawed and/or based on laboratory experiments. We therefore tested if there was heritable variation for FA in bristle and wing traits in three field collections of Drosophila melanogaster by rearing F₁s from field flies under laboratory conditions. One of the collections was reared to the F₂ generation in the laboratory to compare heritability estimates from the laboratory with those from the field-laboratory comparison. Trait means indicated an increase in size under laboratory rearing. FAs increased in one collection, decreased in another collection, and showed no changes in the third collection under laboratory rearing. FAs from the collections tended to converge under laboratory conditions. Morphological traits were heritable under field conditions. However, FA was not significantly heritable for any of the individual traits or when FA was determined by combining traits. Comparisons of the two laboratory generations showed that FA heritability was low under laboratory conditions, in contrast to the morphological traits themselves. These findings suggest a very low heritability for FA in field and laboratory Drosophila. FA in bristle and wing traits may therefore be a poor indicator of genetic quality in Drosophila.     

SIZE-DEPENDENT ASYMMETRY: FLUCTUATING ASYMMETRY VERSUS ANTISYMMETRY AND ITS RELEVANCE TO CONDITION-DEPENDENT SIGNALING

Fluctuating asymmetry (FA) has received much recent attention in studies of the evolution of sexual signaling systems. Tests apparently showing that symmetry decreases as individual condition decreases have bolstered the view that FA plays a significant role in the evolution of sexual signals. However, a closer inspection of several examples of bilateral variation as a function of trait size (a correlate of condition) suggests a different pattern of variation. Rather than FA, these traits suggest a pattern of size-dependent antisymmetry (a bimodal frequency distribution of R – L). We introduce some quantitative methods to test for condition- or size-dependent FA. Our analyses reject pure FA for four of the five published datasets involving signals (the fifth is equivocal), but confirm the presence of size-dependent FA in one nonsignaling trait. In the studies not conforming to FA, the data appear to fit more closely a pattern of antisymmetry in individuals with smaller signaling traits. Our results thus suggest that current discussions and conclusions about the role of FA in the evolution of signaling systems should be reconsidered. More specifically, we note that condition-dependent antisymmetry offers a more reliable indicator than condition-dependent FA. We caution, however, that additional work will be needed to determine whether the pattern is general and not an artifact. Our method of analysis could usefully be applied to studies of other continuous factors expected to be correlated with asymmetries, including heterozygosity, inbreeding, and environmental stress. Finally, we suggest that antisymmetry may have commonly been mistaken for FA in a variety of cases dealing with a variety of problems.     

GEOMETRIC MORPHOMETRICS OF DEVELOPMENTAL INSTABILITY: ANALYZING PATTERNS OF FLUCTUATING ASYMMETRY WITH PROCRUSTES METHODS

Although fluctuating asymmetry has become popular as a measure of developmental instability, few studies have examined its developmental basis. We propose an approach to investigate the role of development for morphological asymmetry by means of morphometric methods. Our approach combines geometric morphometrics with the two-way ANOVA customary for conventional analyses of fluctuating asymmetry and can discover localized features of shape variation by examining the patterns of covariance among landmarks. This approach extends the notion of form used in studies of fluctuating asymmetry from collections of distances between morphological landmarks to an explicitly geometric concept of shape characterized by the configuration of landmarks. We demonstrate this approach with a study of asymmetry in the wings of tsetse flies (Glossina palpalis gambiensis). The analysis revealed significant fluctuating and directional asymmetry for shape as well as ample shape variation among individuals and between the offspring of young and old females. The morphological landmarks differed markedly in their degree of variability but multivariate patterns of landmark covariation identified by principal component analysis were generally similar between fluctuating asymmetry (within-individual variability) and variation among individuals. Therefore there is no evidence that special developmental processes control fluctuating asymmetry. We relate some of the morphometric patterns to processes known to be involved in the development of fly wings.     

THE FITNESS OF MANIPULATING PHENOTYPES: IMPLICATIONS FOR STUDIES OF FLUCTUATING ASYMMETRY AND MULTIVARIATE SELECTION

Phenotypic manipulation (or phenotypic engineering) that alters trait distributions provides a way to increase the statistical power of detecting relationships between traits and fitness. Manipulations relying on plastic responses, however, assume a specific relationship between the perturbation and the alteration of the traits when multiple traits are involved. We measured several traits, including condition measured as fluctuating asymmetry, in the ladybird beetle Harmonia axyridis under six different diets to examine how altered environments affected multiple traits and their distributions. Although diet affected fluctuating asymmetry, we found no consistent relationship between degree of asymmetry and other phenotypic measures. As expected, individual traits were altered by our treatments. Contrary to expectation, relationships among traits were not constant among diets. Our results suggest that assumptions about the relationship between condition and trait values, especially fluctuating asymmetry, cannot be made. Further, studies that use manipulated phenotypes to statistically determine the form of selection must first demonstrate that the pattern of the phenotypic correlation matrix is not itself altered by the manipulation. If the phenotypic correlation matrix is not constant, then experimental estimates of selection coefficients may not reflect selection that occurs in the wild.     

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.     

SIZE AND FLUCTUATING ASYMMETRY OF MORPHOMETRIC CHARACTERS IN MICE: THEIR ASSOCIATIONS WITH INBREEDING AND t-HAPLOTYPE

Abstract Fluctuating asymmetry (FA), a ubiquitous type of asymmetry of bilateral characters, often has been used as a measure of developmental instability in populations. FA is expected to increase in populations subjected to genetic stressors such as inbreeding or environmental stressors such as toxins or parasites, although results have not always been consistent. We tested whether FA in four skeletal size characters and mandible shape was greater in a population of wild‐derived mice reared in the laboratory and subjected to one generation of inbreeding (F = 0.25) versus that in an outbred group (F= 0.00). FA did not significantly differ between the inbred and outbred groups, despite the fact that these two groups differed dramatically in fitness under seminatural population conditions. As far as we know, this is the first study to evaluate the relationship between FA and inbreeding in wild house mice, and our general conclusion is opposite that of earlier work on laboratory inbred strains of mice and their hybrids. Size for two of the characters was significantly less in inbreds than in outbreds, however, and there was a significant difference between inbreds and outbreds in the signed differences of right and left sides in one character (humerus length). Some of the mice in both groups also were heterozygous or homozygous carriers of the t‐complex. Because mice carrying this chromosome 17 variant are known to have reduced fitness, we also tested whether they had greater FA than mice carrying non‐t‐haplotypes. The overall level of a composite FA index calculated from all four characters was in fact significantly higher in the t‐bearing mice. These combined results suggest that FA is not a generally sensitive proxy measure for fitness, but can be associated with fitness reductions for certain genetic stressors.     

SEXUAL SELECTION IN THE BARN SWALLOW (HIRUNDO RUSTICA). IV. PATTERNS OF FLUCTUATING ASYMMETRY AND SELECTION AGAINST ASYMMETRY

The patterns of variation in fluctuating asymmetry were studied in four morphological characters of the barn swallow Hirundo rustica. The level of absolute and relative asymmetry was larger in the secondary sexual character “outer tail length” than in three nonsexual morphological traits (wing, central tail, and tarsus length). The extent of individual asymmetry in outer tail length was negatively correlated with tail-ornament size, whereas the relationship between asymmetry of all other morphological characters and their size was flat or U-shaped. Asymmetry in outer tail length was unrelated to asymmetry in other morphological characters, whereas asymmetries in the length of wing, central tail, and tarsus were positively correlated. Male bam swallows exhibited larger asymmetry in outer tail length than females. Asymmetry of most morphological traits exhibited intermediate repeatabilities between years, with the exception of male and female outer tail length, which were highly repeatable. Tail asymmetry of offspring weakly, though significantly, resembled that of their parents. Asymmetry in wing and outer tail length was also significantly related to several fitness components. Male barn swallows that acquired a mate were less asymmetric in wing and outer tail length than unmated males. Females with more asymmetrical tails laid eggs significantly later. Annual reproductive success was unrelated to fluctuating asymmetry. Male barn swallows that survived were less asymmetric in wing and outer tail length than nonsurvivors, whereas female survivors were less asymmetric in outer tail length than nonsurvivors. These results suggest that levels of fluctuating asymmetry in barn swallows are associated with differences in fitness.     

PHENOTYPIC PLASTICITY AND EPIGENETIC MARKING: AN ASSESSMENT OF EVIDENCE FOR GENETIC ACCOMMODATION

The relationship between genotype (which is inherited) and phenotype (the target of selection) is mediated by environmental inputs on gene expression, trait development, and phenotypic integration. Phenotypic plasticity or epigenetic modification might influence evolution in two general ways: (1) by stimulating evolutionary responses to environmental change via population persistence or by revealing cryptic genetic variation to selection, and (2) through the process of genetic accommodation, whereby natural selection acts to improve the form, regulation, and phenotypic integration of novel phenotypic variants. We provide an overview of models and mechanisms for how such evolutionary influences may be manifested both for plasticity and epigenetic marking. We point to promising avenues of research, identifying systems that can best be used to address the role of plasticity in evolution, as well as the need to apply our expanding knowledge of genetic and epigenetic mechanisms to our understanding of how genetic accommodation occurs in nature. Our review of a wide variety of studies finds widespread evidence for evolution by genetic accommodation.     

FLUCTUATING ASYMMETRY IS NONGENETICALLY RELATED TO MATING SUCCESS IN DROSOPHILA BUZZATII

Abstract To date, there is still no consensus on the real significance of fluctuating asymmetry (FA) in evolutionary biology. Some studies have established links between FA and Darwinian fitness, and in a number of cases intermediate heritabilities for FA have been reported. However, many claims have been raised against the generality of these findings. I therefore tested if FA of a sexually selected trait (wing length) is indeed related to male mating success in Drosophila buzzatii from field and laboratory samples and whether FA has detectable heritability. Single, unsuccessful males had greater asymmetry for wing length than their mating counterparts both in nature and under nonoptimal rearing environments, but the higher FA in single males is most likely due to a poorer average phenotypic condition because there was no evidence of a genetic basis for this trait. Further evidence of an increase in FA under larval food stress is suggested when comparing the magnitude of the FA levels between stressful and optimal environments. On methodological grounds, a linear model is suggested that allows directional asymmetry (DA) and any genetic variation of DA that may be present to be statistically eliminated from estimates of FA.     

FLUCTUATING ASYMMETRY DOES NOT CONSISTENTLY REFLECT SEVERE DEVELOPMENTAL DISORDERS IN HUMAN FETUSES

Developmental instability (DI), as measured by fluctuating asymmetry (FA), may reflect fitness and facilitate the expression of morphological variation. Insights in the underlying mechanisms and magnitude of DI during early development would increase our understanding of its role in evolutionary biology. We studied associations between FA and congenital abnormalities of different origins and functional systems in deceased human fetuses. Major congenital abnormalities corresponded to severe, often-lethal developmental disorders disrupting normal development from early organogenesis onward, but only moderately increased FA. Lower FA with age also supported the hypothesis that more severe abnormalities, leading to an earlier death, increased DI. Although FA related significantly to measures of fitness or health, we anticipated stronger associations because fetal health problems were detrimental. Furthermore, elevated FA occurred in only 4 of 17 disorders (left–right patterning, limb defects, and problems of bronchopulmonary and urogenital system). Fetuses experiencing major abnormalities other than these four types did not show increased FA. This suggests that the functional importance of symmetry in limbs has resulted in strong selection for symmetry and reduced its sensitivity to stress. Finally, the observed patterns suggest that specific developmental pathways have a stronger effect on DI than others do.     

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.     

FLUCTUATING ASYMMETRY IN CENTRAL AND MARGINAL POPULATIONS OF LYCHNIS VISCARIA IN RELATION TO GENETIC AND ENVIRONMENTAL FACTORS

Developmental instability in the form of increased fluctuating asymmetry can be caused by either genetic or environmental stress. Because extinctions can be attributed broadly to these factors, fluctuating asymmetry may provide a sensitive tool for detecting such stresses. We studied the level of fluctuating asymmetry of flowers of a perennial outcrossing plant species, Lychnis viscaria, both in natural and common-garden populations. The degree of flower asymmetry was higher in small, isolated, and marginal populations of the species range. These marginal populations also were the most homozygous. In the core area of the species' range, flowers were more symmetrical The level of asymmetry was correlated with both population size and heterozygosity. However, a partial correlation analysis revealed that when the impact of population size was controlled for, there was a negative relationship between fluctuating asymmetry and heterozygosity, whereas when controlling for heterozygosity, no relationship between population size and fluctuating asymmetry was found. This indicates that genetic consequences of small population size probably underlie the relationship between the level of asymmetry and population size. Results from a transplantation experiment showed that individuals subjected to a higher environmental stress had an increased level of asymmetry compared to control plants. In the common-garden conditions the level of fluctuating asymmetry did not differ between the central and marginal populations. This suggests that presumably both genetic and environmental factors affected to the higher level of asymmetry among marginal populations compared to central ones. In all we conclude that even though fluctuating asymmetry seems to be a sensitive tool for detecting stresses, results from studies focusing on only one factor should be interpreted with caution.     

FLUCTUATING ODONTOMETRIC ASYMMETRY,MORPHOLOGICAL VARIABILITY,AND GENETIC MONOMORPHISM IN THE CHEETAH ACINONYX JUBATUS

The magnitudes of dimensional variability and fluctuating asymmetry in dental dimensions are reported for a sample of South African cheetah Acinonyx jubatus. To test the hypothesis that elevated levels of variability and asymmetry are associated with the increased developmental instability reported for this species, our results were contrasted to those for two other felids: Felis lybica and F. caracal. These findings suggest that dental dimensions in cheetahs are not significantly more variable or asymmetric. Hence, it is concluded that the cheetah may not be as developmentally unstable as was previously supposed.