Patterns of fluctuating asymmetry in developing primary feathers: a test of the compensational growth hypothesis

The study of asymmetry ontogeny may reveal the mechanisms controlling the development of bilaterally symmetrical characters and the causes of asymmetry. In birds, flight feather asymmetries appear to increase at the beginning of growth and decrease at the end of their development. It has been proposed that such a pattern could be proximately caused by a developmental mechanism of compensational growth between the left and right wings, which should act to restore trait symmetry at the end of growth. In this study, I tested the hypothesis of the existence of a mechanism of compensational growth by performing an experiment, which consisted of provoking small asymmetries in the seventh primary feathers of house sparrows (Passer domesticus) by inducing the two feathers (one each side) to moult two days apart. On each side, the feathers grew in a similar way, independently of the growth of the other side. Feather length asymmetries were shortened with the advance of growth. However, the differences in time of growth persisted throughout development. These results do not support the existence of a mechanism of compensational growth. Primary feathers'' asymmetries could decrease at the end of growth because the growth of the two feathers follows a programmed trajectory, which tends towards a certain maximum potential size.     

Feather development under environmental stress: lead exposure effects on growth patterns in Great Tits Parus major

Capsule Regrowth rate of tail feathers is more strongly affected compared to feather length and symmetry.

Aims To assess the value of avian feathers as bioindicators.

Methods The origin and persistence of fluctuating asymmetry (FA) in homologous pairs of regrowing feathers was studied in captive birds under different levels of environmental stress, respresented by exposure to lead (Pb). Homologous feathers of individually housed birds were plucked synchronously or with a delay of seven days. We measured growth rate, regeneration time, final size and FA of regrown feathers and related them to Pb stress.

Results Asymmetry decreased as feathers reached their final length. This was not due to compensatory growth but rather a consequence of the programmed growth trajectory of single feathers. Tail feathers grown under higher Pb pollution showed increased regeneration times, decreased growth rates and shorter lengths, but no changes in development times nor in FA. For differences between both (i) original and induced feathers and (ii) control and Pb treatment, effect sizes of parameters related to feather development (growth bar width, growth rate, regeneration and development time) were consistently larger than those related to the resulting phenotype (feather length and FA).

Conclusions Growth bar widths in particular provide an applicable, sensitive and reliable indicator of adverse conditions such as Pb pollution and experimental conditions. In general, phenotypic characteristics that retrospectively allow estimation of growth rates may be more suitable for monitoring environmental stress than sizes or asymmetries of full-grown traits.     

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 variation and fluctuating asymmetry in sexually dimorphic feather ornaments in relation to sex and mating system

Secondary sexual characters have been hypothesized to demonstrate increased phenotypic variation between and within individuals as compared to ordinary morphological traits. We tested whether this was the case by studying phenotypic variation, expressed as the coefficient of variation (CV), and developmental instability, measured as fluctuating asymmetry (FA), in ornamental and non-ornamental traits of 70 bird species with feather ornamentation while controlling for similarity among species due to common descent. Secondary sexual characters differed from ordinary morphological traits by showing large phenotypic CV and FA. This difference can be explained by the different mode of selection operating on each kind of trait: a history of intense directional (ornaments) and stabilizing selection (non-ornaments). Phenotypic variation is reduced in the sex with more intense sexual selection (males), but does not differ among species with different mating systems. The strength of stabilizing selection arising from natural selection is associated with decreased CV (wing CV is smaller than tarsus or tail CVs). We found evidence of FA being reduced in ornamental feathers strongly affected by aerodynamics (tail feathers) compared to other ornaments, but only in females. In conclusion, CV and FA were not related, suggesting mat phenotypic plasticity and developmental instability are independent components of phenotypic variation.     

POPULATION AND DEVELOPMENTAL VARIATION IN THE FEATHER TIP

Variation among adults reflects variation in basic developmental processes, such as cell division rate. Partitioning the variation into its developmental components would be a major step in understanding evolutionary constraints, but is far from being achieved for any character. In this paper, we examine population variation in the feather tip, a useful structure to study because the history of development is recorded in the adult form. Our goal is to document the variability, and provide a developmentally based explanation for the level of variation observed. Using feathers collected from chicks of a small warbler, we partition population variation into variation attributed to accidents of development (through a consideration of fluctuating asymmetry), and among- and within-family components. Population variation in the earliest formed part of the feather is high (the coefficient of variation is c. 30%); population variation in later formed parts of the feather is lower. The among-individual and developmental noise components are both reduced in later formed parts, but there are differences in the way the two components are associated among the feather parts. The early and later formed parts are highly integrated at the among-individual level (correlations ≈ 1.0) but not at the developmental noise level (correlations ≈ 0.5). This suggests that at least two basic developmental processes are involved in determining the length of the various feather parts. We review feather development and pattern formation models to demonstrate that at least two developmental processes are indeed involved in feather growth. We show how these processes could interact to achieve the relative invariance in the later formed parts of the feather.     

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.     

Heritability of directional and fluctuating asymmetry for mandibular characters in random-bred mice

In bilateral characters, two kinds of asymmetries are common: fluctuating asymmetry (FA), or nondirectional variation between left and right sides, and directional asymmetry (DA), in which one side is consistently larger than the other. FA has been extensively used as a measure of developmental stability because of its presumed environmental basis whereas DA has not typically been recommended because it has been presumed to have at least some genetic basis. To test these two hypotheses, heritabilities were calculated via parent–offspring regression for both DA and FA in 10 triply measured mandible characters in random-bred mice. Midparent estimates of heritabilities of DA in the 10 characters were quite low (mean = 0.06), but significant for one character as well as the sum of the DA values over all characters (0.21). Midparent estimates of heritability of FA in the 10 characters also were low (mean = 0.03), but not significant for any individual character or the sum of the FA values over all characters. Heritabilities of developmental stability calculated from heritabilities and repeatabilities of FA in the mandible characters were higher in magnitude (mean of midparent estimates = 0.45), but all still were not statistically significant. It was concluded that both hypotheses were supported, but that genetic variation in DA was so small that the potential for DA as an indicator of developmental stability should be explored.     

Enzyme heterozygosity,metabolism, and developmental stability

Developmental homeostasis, measured as either fluctuating asymmetry or variance of morphological characters, increases with enzyme heterozygosity in many, but not all, natural populations. These results have been reported forDrosophila, monarch butterflies, honeybees, blue mussels, side-blotched lizards, killifish, salmonid fishes, guppies, Sonoran topminnows, herring, rufous-collared sparrows, house sparrows, brown hares, white-tailed deer, and humans. Because heterozygosity at a few loci can not predict heterozygosity of the entiry genome, these loci must be detecting localized zones that influence the developmental environment. Studies of malate dehydrogenase in honeybees,Apis mellifera, and lactate dehydrogenase in killifish,Fundulus heteroclitus, revealed that developmental homeostasis varied with heterozygosity of individual loci. Heterozygotes differed from homozygotes in fluctuating asymmetry, morphological variance, and in correlations between morphological characters. The protein loci in these studies code for enzymes, and therefore do not directly influence morphological characters. However, some enzymatic loci substantially influence metabolism, and contribute to variation in the amount of energy available for development and growth. This argument can be made most convincingly for the LDH polymorphism in killifish. LDH genotypes differ in enzyme kinetic properties that measure differences in physiological efficiency, and these differences produce measurable and predictable differences in physiology and development. Under environmental conditions which impose a stress upon development, genotypes at these loci may have different amounts of energy available for development, and consequently exhibit different levels of developmental homeostasis.     

Patterns of leaf asymmetry changes in Plantago major L. (ssp. major) natural populations exposed to different environmental conditions

In the present study, developmental stability of leaf traits was examined in three natural populations of Plantago major L. (ssp. major), representing two polluted environments (Karaburma and Zemun) and an unpolluted area (Crni Lug). Developmental stability was assessed as fluctuating asymmetry (FA). The magnitude of FA is believed to reflect differences in the ability of individuals to buffer their development in natural populations. We hypothesized that there are differences within characters and among characters in response to environmental conditions. Significant patterns of asymmetry correlations and asymmetry changes were detected both within characters and between characters. The manova results revealed a significant effect of individual and a significant individual × environment interaction on actual asymmetry (logL_i ? logR_i) and on the amount of asymmetry |(logL_i ? logR_i)| for leaf width and vein distances within a leaf. Over time, statistically significant and positive correlations of the FA values were detected for each trait separately per sample (population). For both leaf traits, there were differences for (logL_i ? logR_i) and |(logL_i ? logR_i)| asymmetry values among individuals within samples in response to yearly variations. Statistically significant and negative correlations for (logL_i ? logR_i) versus |(logL_i ? logR_i)| asymmetries were detected for both leaf traits. In summary, our results highlight the importance of differences in the ability of individuals to buffer their development under different environmental conditions and point to the concept that developmental stability is character specific.     

Parent Barn Swallow fluctuating asymmetry and offspring quality

Fluctuating asymmetry may impair locomotion but may also reflect intrinsic phenotypic quality. I tested whether fluctuating asymmetry of adult Barn Swallows Hirundo rustica negatively influenced offspring quality, by estimating the relationship between parental asymmetry and offspring size, condition and immunocompetence during three breeding seasons. Controlling for timing of breeding, brood size and the size of a secondary sexual character (tail length), wing and outermost tail feather asymmetry of male and female parents was not significantly correlated with offspring size, condition and immunocompetence. This was the case in spite of clear differences in nestling quality among years. In addition, parents with extreme asymmetries due to tail feather damage (not representing fluctuating asymmetry) did not have nestlings of lower quality than parents with undamaged tail feathers. These results indicate that there is only a weak relation between parental asymmetry and offspring quality.     

Fluctuating asymmetry in Sardinian Warblers Sylvia melanocephala inhabiting two shrublands affected by fire

The effects of post-fire changes in vegetation and habitat quality on the developmental stability of individual birds have not been assessed to date. Here we compare fluctuating asymmetry in tail feathers of Sardinian Warblers Sylvia melanocephala inhabiting two shrubby zones, the first burned in both 1982 and 1994 and the second only in 1982. Juveniles with unmoulted rectrices showed significantly higher levels of tail feather asymmetry in the zone burned in 1994. This result is consistent with the hypothesis that recently burned shrublands offer lower quality habitats for this species. Because feather asymmetry was positively and significantly related to the abundance of low shrubs up to 50 cm tall, we suggest that juvenile assessment of habitat quality is primarily based on the structure of the shrub layer.     

Asymmetric size and shape variation in the Central European transect across the house mouse hybrid zone

We studied asymmetric variation of the mandible in the Central European portion of the hybrid zone between two house mouse subspecies, Mus musculus musculus and Mus musculus domesticus. Within introgression classes, defined by the share of diagnostic allozymes, we quantified the directional and fluctuating component of asymmetric variation, as well as skewness and kurtosis of individual asymmetry distributions. Furthermore, in the same manner we re‐analysed asymmetric variation of the ventral side of the skull. According to the quadratic polynomial model, the mandible shape‐fluctuating asymmetry, but not size‐fluctuating asymmetry, was significantly decreased in the centre of the hybrid zone (with a minimum predicted for a hybrid index of 0.41). On the contrary, the skull shape‐fluctuating asymmetry non‐monotonically increased towards the musculus side of the hybrid zone (with a peak predicted for a hybrid index of 0.86). Thus, the impact of hybridization on fluctuating asymmetry is trait‐specific in this portion of the house mouse hybrid zone. The only general feature of asymmetric variation we observed was the shift towards the platykurtosis of asymmetry distributions in the centre of the hybrid zone. Taken together, we suggest genetic variability for right–left asymmetries to be generally increased, but the developmental instability of mandible shape to be decreased, by hybridization. We hypothesize the decrease of developmental instability to be caused by overdominant effects on developmental dynamics rather than by increased heterozygosity. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 13–27.     

Evolution of morphological integration: developmental accommodation of stress-induced variation

Extreme environmental change during growth often results in an increase in developmental abnormalities in the morphology of an organism. The evolutionary significance of such stress-induced variation depends on the recurrence of a stressor and on the degree to which developmental errors can be accommodated by an organism's ontogeny without significant loss of function. We subjected populations of four species of soricid shrews to an extreme environment during growth and measured changes in the patterns of integration and accommodation of stress-induced developmental errors in a complex of mandibular traits. Adults that grew under an extreme environment had lower integration of morphological variation among mandibular traits and highly elevated fluctuating asymmetry in these traits, compared to individuals that grew under the control conditions. However, traits differed strongly in the magnitude of response to a stressor--traits within attachments of the same muscle (functionally integrated traits) had lower response and changed their integration less than other traits. Cohesiveness in functionally integrated complexes of traits under stress was maintained by close covariation of their developmental variation. Such developmental accommodation of stress-induced variation might enable the individual's functioning and persistence under extreme environmental conditions and thus provides a link between individual adaptation to stress and the evolution of stress resistance.     

ANALYSIS OF GENOTYPIC DIFFERENCES IN DEVELOPMENTAL STABILITY IN ANNONA CHERIMOLA

The genetic basis of developmental stability, measured as asymmetry (fluctuating asymmetry in leaves), was analyzed in leaves and flowers of cherimoya (Annona cherimola Mill) and atemoya (A. cherimola × A. squamosa). The individuals analyzed belonged to a controlled collection of cultivars (clones) that had previously been characterized by means of isozymes. We used a nested design to analyze the differences in asymmetry at several sampling levels: individual leaves and flowers, individual trees, and genotypes. The clonal repeatability of developmental stability was not significantly different from zero, thus suggesting the absence of heritability of the asymmetry for leaves and flowers under these environmental conditions. No relationship between asymmetry and individual heterozygosity was found, but leaf fluctuating asymmetry was significantly related to particular isozymic genes. Petal and leaf size showed a phenotypically plastic response to the exposure zone of the tree (mainly due to light). Leaf fluctuating asymmetry also showed such a plastic response. No significant correlation was found between asymmetry and any pomological characters (some of these being fitness related). Finally, the hybrid species (atemoya) did not show larger developmental instability than did the parental species (cherimoya). All these data show that cherimoya asymmetry reveals the random nature of developmental noise, with developmental stability for leaves being possibly related to specific chromosome regions, but with weak evidence for genotypic differences in developmental stability.     

DEVELOPMENTAL STABILITY, DISEASE AND MEDICINE

Developmental stability reflects the ability of a genotype to undergo stable development of a phenotype under given environmental conditions. Deviations from developmental stability arise from the disruptive effects of a wide range of environmental and genetic stresses, and such deviations are usually measured in terms of fluctuating asymmetry and phenodeviants. Fluctuating asymmetry is the most sensitive indicator of the ability to cope with stresses during ontogeny. There is considerable evidence that developmental stability, and especially fluctuating asymmetry, is a useful measure of phenotypic and genetic quality, because it covaries negatively with performance in multiple fitness domains in many species, including humans. It is proposed that developmental stability is an important marker of human health. Our goal is to initiate formally the integration of the sciences of evolutionary biology, developmental biology and medicine. We believe that this integrative framework provides a significant addition to the growing field of Darwinian medicine. The literature linking developmental stability and disease in humans is reviewed. Recent biological theoretical treatments pertaining to developmental stability are applied to a range of human health issues such as genetic diseases, ageing and survival, subfertility, abortion, child maltreatment by parents, cancer, infectious diseases, physiological and mental health, and physical attractiveness as a health certification.     

Individual variation in growth trajectories: phenotypic and genetic correlations in ontogeny of the house finch (Carpodacus mexicanus)

We studied patterns of growth in a recently established natural population of the house finch (Carpodacus mexicanus) to examine whether phenotypic and genetic covariation among age‐specific trait values is likely to constrain morphological change favoured by selection acting on adults. We found variable patterns of allometric relationships during ontogeny, and documented relatively weak covariations among ages or among traits in individual growth trajectories. Frequent compensatory growth largely cancelled out the initial differences among nestlings, potentially enabling house finches to raise offspring under diverse and unpredictable environmental conditions. Moderate levels of additive genetic variance in morphological traits throughout ontogeny, and relatively low and fluctuating phenotypic and genetic covariation among ages imply strong potential for evolutionary change in morphological traits under selection. This conclusion is consistent with the profound population‐level divergence in morphological patterns that accompanied very successful colonization of most of North America by the house finch over the last 50 years.     

Why do some traits show higher fluctuating asymmetry than others? A test of hypotheses with tail feathers of birds

Certain characters are more susceptible to increased fluctuating asymmetry (FA) than others. This trait-specific susceptibility has normally been attributed to different degrees of developmental stability, which could be caused by different modes of selection, functionality, or the stress experienced during the development process. Recently, it has also been suggested that the expression of FA not only depends on developmental stability, but also on the cost of growth of the trait, defined as the amount of structural components necessary to form a unit of length of a given character. In accordance with this argument, a trait with more structural components per unit of length should show lower asymmetry than a simpler one. To test this hypothesis, we examine the structure (number of barbs, barb length, and rachis width) and asymmetry of the longest tail feathers in 26 bird species. Regression analyses using phylogenetically independent contrasts show that FA is negatively correlated with the number of barbs and feather rachis width in males (including species with elongated tails subjected to sexual selection), and with rachis width in females, whose tails supposedly evolve by natural selection. Moreover, the negative correlation between FA and rachis width persisted when taking only the males of non-dimorphic species. These results confirm the hypothesis, suggesting that a trait's susceptibility to express developmental instability by fluctuating asymmetry depends on its structural composition.     

Fluctuating asymmetries and reproductive success in the peacock blenny

In an investigation of the relationship between reproductive success and fluctuating asymmetry (FA) in the peacock blenny Salaria pavo , FA was measured in four bilaterally paired characters in successful and unsuccessful males during the breeding season. Reproductive success among successful males was assessed by calculating the number of eggs the males were defending. Absolute FA values relative to trait size were high for all characters and it is suggested that this could be a consequence of sub-optimal environmental conditions. Two of the traits presented higher absolute FA values suggesting a lower canalization during ontogeny. No difference in FA between successful and unsuccessful males was found and no relationship between FA and number of eggs among the successful males occurred for any of the measured traits. A composite index of FA, that should better reflect overall developmental competence, was also unrelated to reproductive success. These results indicate that FA is not associated with reproductive success among males of S. pavo . Successful males were larger than unsuccessful males and a strong positive correlation was detected between the body length of the parental males and the number of eggs they had in the nest, even when controlling for the internal nest area. Body size may give males a reproductive advantage by being preferred by females and by having an advantage in male-male competition for nests of higher quality.     

Jamaican Symmetry Project: long-term study of fluctuating asymmetry in rural Jamaican children.

Fluctuating asymmetry, small deviations from perfect bilateral symmetry, is negatively correlated with health and positively correlated with sexual selection in human adults, but the accumulation, persistence, and fitness implications of asymmetries during childhood are largely unknown. Here, we introduce the Jamaican Symmetry Project, a long-term study of fluctuating asymmetry and its physical and behavioral correlates in rural Jamaican children. The project is based on an initial sample of 285 children (156 boys and 129 girls), aged 5 to 11 years. We describe the design of the project and the methodology of measuring 10 paired morphometric traits. All traits except hand width showed fluctuating asymmetry. Fluctuating asymmetries of the legs tended to be related and were less than half as great as fluctuating asymmetries of the arms and ears. Therefore the legs may show high developmental stability resulting from selection for mechanical efficiency. A fluctuating asymmetry composite score revealed that boys have significantly lower fluctuating asymmetry than girls and that this effect resides mainly in the elbows. There were significant positive relationships between composite fluctuating asymmetry and age, height, and weight, but multiple regression analyses showed that age was negatively related to fluctuating asymmetry, whereas body size was positively correlated. These findings are compared with results from recent English studies.     

Fluctuating asymmetry inMacaca fascicularis: A study of the etiology of developmental noise

Fluctuating asymmetry was determined for six cranial measurements in an age-diverse sample of 138 individuals ofMacaca fascicularis. These data were used to choose among four hypotheses concerning the etiology of developmental noise. The hypotheses considered are (1) that developmental noise represents asymmetry in the causal history of a developing organism's interaction with the environment, (2) that it represents stochasticity in the mechanics of growth and induction, (3) that it reflects variation in the initial conditions of a developmental process, and (4) that it represents the random accumulation of noise at a level below that of morphogenetic mechanism. These hypotheses were tested against predictions concerning the intraspecific patterning of fluctuating asymmetry against age and size and the covariation of asymmetry values. Only the predictions of the fourth hypothesis were confirmed by results of this study. These results provide evidence for the view that developmental noise, as reflected by fluctuating asymmetry, is an intrinsic property of developmental systems, and not merely produced by the complexity of the organism's interaction with the environment.