Developmental stability,sexual selection and speciation

Fluctuating asymmetry occurs when an individual is unable to undergo identical development of an otherwise bilaterally symmetric trait on both sides of its body. Since both sides of a bilaterally symmetric trait are the result of the actions of a single genome, fluctuating asymmetry represents an epigenetic measure of the sensitivity of development to stress. Different morphological traits may show a direct relationship between their functional importance and their degree of developmental canalization. This may explain why some characters show high degrees of fluctuating asymmetry, and why these characters more often become exaggerated secondary sexual ornaments. The degree of fluctuating asymmetry is generally larger in small marginal populations living in novel environments, and this will particularly lead to relatively large degrees of asymmetry in the least developmentally canalized traits. More stringent selection against heterozygotes in marginal populations may further break down developmental stability and linkage groups which would lead to increased genetic variance. Females may prefer to mate with males having large, but relatively symmetric morphological characters, because it is more difficult to make large traits (a good genes argument), a large trait is more easily perceived (a sensory bias preference), and because symmetry signals ability to cope with stress (a good genes argument). The low degree of developmental stability and the large amount of genetic variance in secondary sexual characters in small, marginal populations could set the scene for rapid development of divergence and speciation in marginal populations.     

Patterns of fluctuating asymmetry in sexual ornaments predict female choice

Extravagant secondary sexual characters are assumed to have arisen and be maintained by sexual selection. While traits like horns, antlers and spurs can be ascribed to intrasexual competition, other traits such as extravagant feather ornaments, displays and pheromones have to be ascribed to mate choice. A number of studies have tested whether females exert selection on the size of male ornaments, but only some of these have recorded female preferences for the most extravagantly ornamented males. Here I demonstrate that female choice can be directly predicted from the relationship between the degree of fluctuating asymmetry and the size of a secondary sexual character. Fluctuating asymmetry is an epigenetic measure of the ability of individuals to cope with stress, and it occurs when an individual is unable to undergo identical development of an otherwise bilaterally symmetric trait on both sides of its body. There is a negative relationship between the degree of fluctuating asymmetry and the absolute size of an ornament in those bird species with a female preference for the largest male sex trait, while there is a flat or U-shaped relationship among species without a female preference. These results suggest that females prefer exaggerated secondary sexual characters if they reliably demonstrate the ability of males to cope with genetic and environmental stress. Some species may demonstrate a flat or U-shaped relationship between the degree of fluctuating asymmetry and the absolute size of an ornament because (i) the genetic variance in viability signalled by the secondary sex trait has been depleted; (ii) the secondary sex trait is not particularly costly and therefore does not demonstrate condition dependence; or because (iii) the sex traits can be considered arbitrary traits rather than characters reflecting good genes.     

INHERITANCE OF MERISTIC VARIATION AND THE EVOLUTION OF DEVELOPMENTAL STABILITY IN RAINBOW TROUT

We found relatively high heritabilities in the narrow sense for seven of eight meristic characters in a population of rainbow trout using regression of mean progeny values on mid-parent values. In sharp contrast, there is no statistically significant additive genetic variance controlling developmental stability, as measured by fluctuating asymmetry (h² = 0.02). However, there is a significant correlation between the average heterozygosity of each family at isozyme loci and the average number of asymmetric traits per individual. We have previously reported a strong correlation between heterozygosity at protein loci and decreased fluctuating asymmetry in this and other salmonid populations. Thus, there is little or no additive, but substantial dominance, genetic variation affecting fluctuating asymmetry. This suggests that there has been directional selection for increased developmental stability.     

A meta-analysis of the heritability of developmental stability

The existence of additive genetic variance in developmental stability has important implications for our understanding of morphological variation. The heritability of individual fluctuating asymmetry and other measures of developmental stability have frequently been estimated from parent-offspring regressions, sib analyses, or from selection experiments. Here we review by meta-analysis published estimates of the heritability of developmental stability, mainly the degree of individual fluctuating asymmetry in morphological characters. The overall mean effect size of heritabilities of individual fluctuating asymmetry was 0.19 from 34 studies of 17 species differing highly significantly from zero (P < 0.0001). The mean heritability for 14 species was 0.27. This indicates that there is a significant additive genetic component to developmental stability. Effect size was larger for selection experiments than for studies based on parent-offspring regression or sib analyses, implying that genetic estimates were unbiased by maternal or common environment effects. Additive genetic coefficients of variation for individual fluctuating asymmetry were considerably higher than those for character size per se. Developmental stability may be significantly heritable either because of strong directional selection, or fluctuating selection regimes which prevent populations from achieving a high degree of developmental stability to current environmental and genetic conditions.     

Fluctuating asymmetry and genetic variability in the roe deer (Capreolus capreolus): a test of the developmental stability hypothesis in mammals using neutral molecular markers

Fluctuating asymmetry (FA), used as an indicator of developmental stability, has long been hypothesized to be negatively correlated with genetic variability as a consequence of more variable organisms being better suited to buffer developmental pathways against environmental stress. However, it is still a matter of debate if this is due to metabolic properties of enzymes encoded by certain key loci or rather to overall genomic heterozygosity. Previous analyses suggest that there might be a general difference between homeo- and poikilotherms in that only the latter tend to exhibit the negative correlation predicted by theory. In the present study, we addressed these questions by analysing roe deer (Capreolus capreolus) from five German populations with regard to FA in metric and non-metric skull and mandible traits as well as variability at eight microsatellite loci. Genetic variability was quantified by heterozygosity and mean d2 parameters, and although the latter did not show any relationship with FA, we found for the first time a statistically significant negative correlation of microsatellite heterozygosity and non-metric FA among populations. Because microsatellites are non-coding markers, this may be interpreted as evidence for the role of overall genomic heterozygosity in determining developmental stability. To test if the threshold character of non-metric traits is responsible for the metric vs non-metric difference we also carried out calculations where we treated our metric traits as threshold values. This, however, did not yield significant correlations between FA and genetic variability either.     

Fluctuating asymmetry and sexual selection

Fluctuating asymmetry occurs when an individual is unable to undergo identical development on both sides of a bilaterally symmetrical trait. Fluctuating asymmetry measures the sensitivity of development to a wide array of genetic and environmental stresses. We propose that fluctuating asymmetry is used in many signalling contexts for assessment of an individual's ability to cope with its environment. We hypothesize that fluctuating asymmetry is used in sexual selection, both in fighting and mate choice, and in competition for access to resources. Evidence is reviewed showing that the patterns of fluctuating asymmetry in secondary sexual characters differ from those seen in other morphological traits. Secondary sexual characters show much higher levels of fluctuating asymmetry. Also, there is often a negative relationship between fluctuating asymmetry and the absolute size of ornaments, whereas the relationship is typically U-shaped in other morphological traits. The common negative relationship between fluctuating asymmetry and ornament size suggests that many ornaments reliably reflect individual quality.     

Geography of fluctuating asymmetry in the greenfinch, Carduelis chloris

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

Fluctuating and directional asymmetry in natural bird populations exposed to different levels of habitat disturbance, as revealed by mixture analysis

While bilateral trait asymmetry is widely recognized to estimate developmental instability, much controversy exists over which types of asymmetry (fluctuating, directional, and/or antisymmetry) to use. Recently it has been hypothesized that the three types are strongly interrelated, and that increased developmental instability may be reflected in a transition from fluctuating to directional asymmetry and/or antisymmetry. Alternatively, habitat disturbance might change the genetic expression of directional asymmetry. We present herein the first empirical evidence for stress-mediated shifts in types of asymmetry in natural populations, by using mixture analysis to model tarsus asymmetry in bird populations exposed to different levels of habitat disturbance. Observed asymmetry patterns almost exclusively consisted of true fluctuating asymmetry in the least disturbed populations, but became progressively mixed with directional asymmetry under increasing disturbance. Failing to unravel these mixtures of different forms of asymmetry may have critical implications for the analysis and interpretation of asymmetry data.     

Developmental instability in Brassica campestris (Cruciferae): fluctuating asymmetry of foliar and floral traits

The degree of fluctuating asymmetry of bilateral traits provides a measure of developmental instability, which can be influenced by genetic as well as environmental stress. We studied genetic variation between and within two populations of the mustard Brassica campestris for asymmetry of foliar (cotyledon width) and floral (petal length and width) traits as well as for phenological (germination and flowering) and performance (biomass and flowering) traits. The two populations differed in mean expression of most traits, including asymmetry. However, within-population estimates of genetic variability tended to be lower for asymmetry than other traits. Asymmetry was greater in the population that had lower biomass accumulation and flower production, which supports the idea that population-level asymmetry may be indicative of population-level performance. However, within each population, evidence that performance was negatively correlated with asymmetry was equivocal. Within populations there was little or no concordance among estimates of asymmetry based on different structures, i.e., plants that had highly asymmetrical cotyledons did not tend to have highly asymmetrical petals. The lack of a general buffering capacity at the individual level may be explained by developmental processes (e.g., action of different genes or morphogens) as well as evolutionary processes (e.g., selection on asymmetry of different traits).     

Non-metric variation of the skull in samples of four Indian populations

Four skeletal samples from the states of Uttar Pradesh, Bihar, and Andhra Pradesh in India are compared using cranial non-metric traits. The skeletal “epigenetic” distances correspond with the geographic pattern of separation, also demonstrating variable correspondence with known genetic relationships of the living populations.     

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.     

Sexual selection, stabilizing selection and fluctuating asymmetry in two populations of pupfish (Cyprinodon pecosensis)

Fluctuating asymmetry of morphological traits is thought to reflect the capacity of a genotype to produce an integrated, functional phenotype. I tested three predictions. (1) In a polygynous breeding system, under intense sexual selection on males, breeding males should show greater symmetry in bilaterally symmetrical traits than non-breeding males or females. (2) If these traits are under stabilizing selection, highly symmetrical individuals also should be modal phenotypes, thus near the mean value for that trait, whereas individuals with increased asymmetry should represent marginal phenotypes, near the extremes of the distribution for that trait. (3) Differences in the intensity of sexual selection should be reflected in differences in the degree of fluctuating asymmetry between sexes among populations. I examined the relationship between male breeding status and the degree of fluctuating asymmetry of four bilaterally symmetrical- traits, preorbital and preopercular pores and pectoral and pelvic fin rays, in two populations of Pecos pupfish which differed in the intensity of sexual selection. These traits do not function in male-male competition or female choice, thus are not directly affected by sexual selection. In Mirror Lake breeding males, as a group, were most symmetrical for all four traits, while non-breeding males and females showed higher levels of fluctuating asymmetry. Similarly, symmetrical individuals also represented modal phenotypes for four traits (breeding males), and for three traits (non-breeding males and females). These patterns were not seen in the Lake Francis population, where breeding males were as asymmetrical as non-breeding males and females, and the degree of fluctuating symmetry did not differ between modal and marginal phenotypes for any of the four traits. When ecological conditions favour intense sexual selection, either through female choice, male-male competition, or both, breeding males represent the most fit phenotypes. Thus sexual selection reinforces the effects of stabilizing selection on characters that do not function as secondary sexual traits. However, when sexual selection is relaxed, differences between sexes disappear.     

Fluctuating asymmetry and inbreeding in Scandinavian gray wolves (Canis lupus)

We investigated fluctuating asymmetry in 13 traits of the skulls and jaws of historical and contemporary populations of Scandinavian gray wolves (Canis lupus). We hypothesized that there is a higher level of fluctuating asymmetry in the inbred contemporary population than in the historical population. Our analyses did not detect any difference in the level of fluctuating asymmetry as predicted. We propose different explanation for this lack of change in fluctuating asymmetry. It is assumed that a large number of studies have failed to find a positive correlation between the level of genetic stress and developmental instability and have therefore never been published, which hampers a good understanding of fluctuating asymmetry as an indicator of developmental instability. The current study is thus important in this context. The gray wolf population in Scandinavia is characterized by an extreme bottleneck followed by two and a half decades of strong inbreeding, but no associated change in fluctuating asymmetry is detected.     

Relationships between non-metric skeletal traits and cranial size and shape.

A long-standing controversy exists about the comparative utility of metric and non-metric traits as biological indicators in population studies. We hypothesize that the underlying scale which determines the presence or absence of a cranial non-metric trait is an expression of general and/or local size variation in the cranium. Therefore metric and non-metric traits will share a common developmental determination. The hypothesis implies that the underlying scale of a non-metric trait will be correlated with measures of cranial size and shape. Forty-eight cranial metric and twenty-five cranial non-metric traits were scored on the left side of adult male crania from four North American Indian populations. New threshold traits were generated for each non-metric trait by dichotomizing discriminant scores produced by discriminant function analysis. The discriminant analysis was performed using metric traits to discriminate between groups formed by non-metric trait presence or absence. Every non-metric trait tested was significantly correlated with its threshold trait in at least one population. The correlations were of moderate to high levels depending on the trait and population sample studied. This implies that metric and non-metric traits share a moderate to high degree of developmental determination. The cause of these correlations may lie in the common effects that growth and development of the soft tissue and functional spaces of the cranium exert on both metric and non-metric traits.     

Fluctuating asymmetry in mice and rats: evaluation of the method

Fluctuating asymmetry, which reflects small, random deviations from symmetry in otherwise bilaterally symmetrical characters, may be used as an indicator of developmental instability in humans and farm animals, and it may also be applicable as a stress indicator. We intended to find a method to allow the use of fluctuating asymmetry as a stress indicator in laboratory animals. That method had to be reproducible and reliable. Furthermore, its applicability in laboratory animals would be improved if it was possible to obtain measurements on the skin surface that correlated with results obtained by measuring the skeleton directly. Seven traits in mice and five traits in rats were evaluated for their applicability for measuring fluctuating asymmetry in mice and rats. Two out of the seven traits, i.e. the width of the joint between the third metatarsal bone and the digital bone on the hind paw, and the length of the incisor tooth at the top, were found to be reliable and reproducible for detecting fluctuating asymmetry in mice as well as in rats. Three out of the seven traits, i.e. the width of the carpal bones, the width of the joint between the tibia and the tarsal bones, and the length of the incisor tooth at the bottom, did express fluctuating asymmetry, but showed a poor day-to-day reproducibility. If the day-to-day reproducibility could be increased, these three traits might also be suitable for measuring fluctuating asymmetry in mice and rats. The last two traits, i.e. the length of ulna and the length of calcaneus plus metatarsal bone i.v., measured both on the skin surface and directly on the bone, did not express fluctuating asymmetry, and had a poor day-to-day reproducibility. These two traits are not suitable for measuring fluctuating asymmetry in mice and rats.     

Genetic and phenotypic correlation between fluctuating asymmetry and two measurements of fear and stress in chickens

The purpose of the present study was to estimate the genetic and phenotypic correlation between fluctuating asymmetry and two measurements of fear and stress in chickens which had not deliberately stressed in any way, using the restricted maximum likelihood procedure. A total of 1073 36-week-old birds from two generations with complete pedigree of the Quail Castellana breed was used. Fluctuating asymmetry of several traits (leg, wing, and feather lengths, and ear-lobe and wattle areas), tonic immobility duration (indicator of fear), and heterophil to lymphocyte ratio (indicator of stress) were measured. The estimated genetic relationship between relative fluctuating asymmetry for the different traits and tonic immobility tended to be positive, that between the combined relative asymmetry of all traits and tonic immobility being near to +1; no significant phenotypic relationship was found between relative fluctuating asymmetry and tonic immobility. The genetic relationship between relative fluctuating asymmetry and heterophil to lymphocyte ratio was not consistent across the traits, ranging from +1 to −1, although the genetic correlation between the combined relative asymmetry and the heterophil to lymphocyte ratio was near to +1 too; no significant phenotypic relationship was found between relative fluctuating asymmetry and heterophil to lymphocyte ratio either. Relative fluctuating asymmetry and body weight were genetically negatively correlated for leg length and ear-lobe area but positively for feather length; the genetic correlation between the combined relative asymmetry and the body weight being near to −1; phenotypic relationships were not significantly different from zero. A significant negative genetic correlation between tonic immobility and heterophil to lymphocyte ratio was found, although the phenotypic association between these two measurements was zero. Phenotypic correlations always near to zero suggest that fluctuating asymmetry was not associated with duration of tonic immobility and heterophil to lymphocyte ratio in birds that have not been deliberately stressed.     

Genetic variability and fluctuating asymmetry of morphological signs of Drosophila melanogaster during development in a pesticide-containing environment

The effects of chlorine-organic insecticide endosulfane (thiodan) on phenotypic and genetic variation in four morphological traits of Drosophila melanogaster (wing length, thorax length, the number of orbital bristles and the number of sternopleural bristles) were examined. In addition, the effect of this pesticide on stability of development measured as fluctuating asymmetry of bilateral traits was estimated. On the medium with endosulfane, phenotypic variation of morphometric traits was significantly higher. No difference in fluctuating asymmetry between the stressed and the control samples was found. The among-line variance of morphometric traits of flies reared on the endosulfane-containing medium was significantly higher as compared to the corresponding variance under control conditions. The efficiency of using fluctuating asymmetry and phenotypic variation of morphometric and meristic traits as indicators of environmental stress in insect populations is discussed.     

Inbreeding reduces power-law scaling in the distribution of fluctuating asymmetry: an explanation of the basis of developmental instability

The study of fluctuating asymmetry has been controversial because of conflicting results found in much of the primary literature. It has been suggested that the source of this conflict is the fact that the basis of fluctuating asymmetry is poorly understood and that, as a consequence, methodology of fluctuating asymmetry studies may be flawed. A new model for the phenomenological basis of fluctuating asymmetry, that variation in fluctuating asymmetry is in large part due to the random exponential growth of cell populations (geometric Brownian motion) that are terminated randomly around a genetically programmed development time, is presented here. If termination of development has a genetic component, then scaling effects and kurtosis in the distribution of fluctuating asymmetry should increase with genetic redundancy of the population. This model prediction was tested by comparing the distribution of multivariate size and shape fluctuating asymmetry in large samples collected from both wild populations and four moderately inbred lines of Drosophila simulans. It was found that while wild populations were best described by a lognormal distribution with power-law scaled tails, the inbred lines derived from the wild stock were dramatically normalized (half-normal) in three of four cases. As predicted, the scaling exponent of the upper tail of the distribution of fluctuating asymmetry increased with inbreeding while the kurtosis and mean fluctuating asymmetry decreased with inbreeding. The model suggests an additional explanation of leptokurtosis in fluctuating asymmetry. Kurtosis and scaling of the statistical distribution of fluctuating asymmetry in a population is related directly to genetic differences between individuals and these differences affect their ability to buffer the process of development against random perturbations.     

Genetic Variability and Fluctuating Asymmetry of Morphological Traits in Drosophila melanogasterReared on a Pesticide-Containing Medium

The effects of chlorine-organic insecticide endosulfane (thiodan) on phenotypic and genetic variation in four morphological traits of Drosophila melanogaster(wing length, thorax length, the number of orbital bristles and the number of sternopleural bristles) were examined. In addition, the effect of this pesticide on stability of development measured as fluctuating asymmetry of bilateral traits was estimated. On the medium with endosulfane, phenotypic variation of morphometric traits was significantly higher. No difference in fluctuating asymmetry between the stressed and the control samples was found. The among-line variance of morphometric traits of flies reared on the endosulfane-containing medium was significantly higher as compared to the corresponding variance under control conditions. The efficiency of using fluctuating asymmetry and phenotypic variation of morphometric and meristic traits as indicators of environmental stress in insect populations is discussed.     

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.