Development of fluctuating asymmetry in tail feathers of the barn swallow Hirundo rustica

Fluctuating asymmetry represents usually small, random deviations from symmetry in bilateral morphological characters. The ontogeny of asymmetry in morphological characters may reveal information about developmental processes in a general sense. I studied the development of fluctuating asymmetry in feather characters of the barn swallow Hirundo rustica, that are developed repeatedly during the single annual moult, with the following results. First, the side developing a larger feather was found to be partially biased, as demonstrated by one side consistently developing a larger feather under natural and experimentally induced growth episode events. Second, asymmetric feathers were found to consist of asymmetric daily growth increments, and the size of the increments developing under different environmental conditions were positively correlated. Third, fluctuating asymmetries of feathers developing under different environmental conditions were positively correlated, although the level of asymmetry was larger under adverse environmental conditions. Fourth, individual asymmetries in tail length and growth bar length were unrelated to the duration of the developmental period, although late growth increments were smaller and more symmetric than early increments. These observations suggest that fluctuating asymmetry partially arises as a consequence of a random bias in the feather follicles and differences in environmental conditions during ontogeny of feathers.     

THE ONTOGENY OF ASYMMETRY IN EARWIG FORCEPS

Fluctuating asymmetry may play an important role in the evolution of naturally selected and secondary sexual traits. However, very little is known about how asymmetries arise or how organisms maintain symmetry during development. Here I propose three mutually exclusive patterns for the development of asymmetries through consecutive growth stages: (1) compensatory growth, in which growth of the shorter side is greatest at the following growth stage; (2) persistent growth, in which growth of the longer side is greatest at the following growth stage; and (3) uncorrelated growth in which growth of the following stage is unrelated to the asymmetry at the previous one. I followed the growth in the forceps of male earwigs through four successive instars. Dyar's rule was used as a null model of insect growth. In the molt from the second to third instar, asymmetries increased through uncorrelated growth and with the magnitude but not the sign expected from Dyar's rule. However, following this, at the molts between instars 3–4 and 4–5, compensatory growth maintained asymmetries at a lower level than expected from Dyar's rule. Although there was no reduction in the absolute magnitude of asymmetry, relative asymmetry did decline. The net growth of forceps length did not follow Dyar's rule. The interpretation of patterns of growth were more sensitive and informative than the interpretation of the relations between asymmetries at consecutive instars.     

Decrease of fluctuating asymmetry among larval instars in an aquatic, holometabolous insect

The use of fluctuating asymmetry (FA) to reveal environmental stress in natural populations has been investigated extensively over the past decade. In aquatic ecosystems, many investigations involve amphibiotic insects with larval development stages in freshwater. To explain the important variability in study results, we investigated the FA level of a natural Hydropsyche exocellata (Insecta: Trichoptera) population at four different stages, from first larval instar to adult. The level of FA decreased between larval stages, but remained constant between the last larval instar and the adult. The presence of a compensational growth mechanism and the elimination of asymmetric individuals by natural selection are two hypotheses that could explain this observation.     

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.     

Dispersal without errors: symmetrical ears tune into the right frequency for survival

Vertebrate animals localize sounds by comparing differences in the acoustic signal between the two ears and, accordingly, ear structures such as the otoliths of fishes are expected to develop symmetrically. Sound recently emerged as a leading candidate cue for reef fish larvae navigating from open waters back to the reef. Clearly, the integrity of the auditory organ has a direct bearing on what and how fish larvae hear. Yet, the link between otolith symmetry and effective navigation has never been investigated in fishes. We tested whether otolith asymmetry influenced the ability of returning larvae to detect and successfully recruit to favourable reef habitats. Our results suggest that larvae with asymmetrical otoliths not only encountered greater difficulties in detecting suitable settlement habitats, but may also suffer significantly higher rates of mortality. Further, we found that otolith asymmetries arising early in the embryonic stage were not corrected by any compensational growth mechanism during the larval stage. Because these errors persist and phenotypic selection penalizes asymmetrical individuals, asymmetry is likely to play an important role in shaping wild fish populations.     

Lateralized tool use in wild New Caledonian crows

Many vertebrate species exhibit sensory and motor asymmetries. Laterality studies of tool use have focused on primates, where hemispheric asymmetries, manifested behaviourally in hand preferences, are thought to be associated with complex motor tasks. Here we report strong individual lateralization for tool use in birds. New Caledonian crows, Corvus moneduloides, hold stick tools with their bills while foraging, often with the nonworking end laterally positioned on one side of the head and the working end possibly positioned in the binocular field. We observed four wild crows to determine whether tools were consistently held on one side. All crows showed a significant preference (two right, two left). This preference was independent of any asymmetry in tool manufacture and held for artificial holes similarly accessible for tools held on either side. This is the first demonstration of lateralized tool use in a nonprimate. In addition, all 173 tools used unilaterally were held only on a crow's preferred side. Such pronounced individual laterality for tool use in natural conditions has previously been reported only in humans and chimpanzees.     

Left–right asymmetries and shape analysis on Ceroglossus chilensis (Coleoptera: Carabidae)

Bilateral symmetry is widespread in animal kingdom, however most animal can deviate from expected symmetry and manifest some kind of asymmetries. Fluctuating asymmetry is considered as a tool for valuating developmental instability, whereas directional asymmetry is inherited and could be used for evaluating evolutionary development. We use the method of geometric morphometrics to analyze left/right asymmetries in the whole body, in two sites and totally six populations of Ceroglossus chilensis with the aim to infer and explain morphological disparities between populations and sexes in this species. In all individuals analyzed we found both fluctuating asymmetry and directional asymmetry for size and shape variation components, and a high sexual dimorphism. Moreover a high morphological variability between the two sites emerged as well. Differences in diet could influence the expression of morphological variation and simultaneously affect body sides, and therefore contribute to the symmetric component of variation. Moreover differences emerged between two sites could be a consequence of isolation and fragmentation, rather than a response to local environmental differences between sampling sites.     

Fluctuating dental asymmetry: Variation among skeletal populations

Recent investigations have shown that nongenetic, environmental factors can adversely affect dental growth and produce bilateral asymmetries in tooth size. When asymmetries do not favor either side, i.e., absence of directional asymmetry, the condition is termed fluctuating asymmetry. Fluctuating asymmetry of the mesiodistal and buccolingual dimensions of the total permanent dentition was compared among human skeletal populations which differ socio-economically and nutritionally. Odontometric data were collected from prehistoric hunters (Indian Knoll site), later aboriginal farming groups (Campbell and Larson sites), and a modern cadaver population (Hamann-Todd). The magnitude of asymmetry is expressed by the familiar correlation coefficient, r. The proportion, then, of intra-individual variation due to fluctuating asymmetry is equal to 1-r. With Wilcoxon's signed ranks test on the correlation coefficients no significant sex difference was shown within populations. Among groups, though, Indian Knoll was the most odontometrically asymmetrical; moreover, within Indian Knoll, the taller and ostensibly better nourished individuals had larger, less asymmetrical teeth than the shorter individuals. These results suggest that environmentally mediated growth disturbance may be sensitively reflected by dental asymmetry. A population exhibiting other signs of severe growth disturbance, e.g., enamel hypoplasia and Harris lines, was the most dentally asymmetrical.     

Rate of moult affects feather quality: a mechanism linking current reproductive effort to future survival.

Life-history theory proposes that costs must be associated with reproduction. Many direct costs are incurred during breeding. There is also evidence for indirect costs, incurred after breeding, which decrease survival and future reproductive success. One possible indirect cost identified in birds is that breeding activity in some way compromises plumage quality in the subsequent moult. Here we propose a mechanism by which this could occur. Breeding activity delays the start of moult. Birds that start to moult later also moult more rapidly--an effect of decreasing daylength. Could this result in poorer quality plumage? We kept two groups of male European starlings, Sturnus vulgaris, one on constant long days and the other on decreasing daylengths from the start of moult. Decreasing daylengths reduced the duration of moult from 103 +/- 4 days to 73 +/- 3 days (p < 0.0001). Newly grown primary feathers of birds that moulted fast were slightly shorter, weighed less (p < 0.05) and were more asymmetrical. They had a thinner rachis (p < 0.005), were less hard (p < 0.01) and less rigid (p < 0.05). They were also less resistant to wear so that differences in mass and asymmetry increased with time. There was no difference in Young''s modulus. Poorer quality plumage will lead to decreased survival due to decreased flight performance and increased thermoregulatory costs. Thus, reproduction incurs costs through a mechanism that operates after the end of breeding.     

Asymmetry and the menstrual cycle in women

Fluctuating asymmetry (FA) is small random deviations from perfect bilateral symmetry that are thought to accumulate during development. FA is therefore a measure of one component of fitness, that is, developmental stability. This work is not concerned with permanent between-individual differences in asymmetries but rather with temporary within-individual changes in asymmetry that are related to the menstrual cycle (cyclical asymmetry, CA). We present evidence from studies of non-sexually selected traits (ear and digit size) and a sexually selected trait (breast size) that, in characters made up wholly or in part of soft tissue, CA varies across the menstrual cycle in women. It is highest at the beginning and end of the cycle, when women are generally infertile, and low in mid-cycle, when fertility is highest. Furthermore in mid-cycle there is an indication of a transitory (24-hour) increase in CA followed by a substantial decrease, which may indicate ovulation. Temporal changes in CA could therefore be used by males to indicate a female's position in the cycle. We discuss these findings in relation to (1) our understanding of the evolution of human mating systems, (2) the practical implications of these data in the treatment of infertility and to facilitate contraception, and (3) their relevance to exercise and dieting as a means to minimize across-cycle increases in asymmetry.     

Validity of the twitch interpolation technique for the assessment of quadriceps neuromuscular asymmetries

This study examined the validity of the twitch interpolation technique for evaluating side-to-side asymmetries in quadriceps neuromuscular function. Fifty-six subjects with a wide range of asymmetries (19 healthy, 24 with unilateral and 13 with bilateral anterior cruciate ligament reconstruction) took part in the study. Supramaximal electrical paired stimuli were delivered to the quadriceps muscle during and immediately after a maximal voluntary contraction (MVC) of the knee extensors (twitch interpolation technique). MVC torque, voluntary activation and resting doublet-evoked torque were measured separately for the two sides, and percent side-to-side asymmetries were calculated for each parameter. MVC torque asymmetry was plotted against voluntary activation asymmetry and doublet-evoked torque asymmetry, and a multiple regression analysis was also conducted. Significant positive correlations were observed between MVC torque asymmetry and both voluntary activation asymmetry (r = 0.40; p = 0.002) and doublet-evoked torque asymmetry (r = 0.53; p < 0.001), and their relative contribution to MVC torque asymmetry was comparable (r = 0.64; p < 0.001). These results establish the validity of the twitch interpolation technique for the assessment of neuromuscular asymmetries. This methodology could provide useful insights into the contribution of some neural and muscular mechanisms that underlie quadriceps strength deficits.     

Directional asymmetry in the limbs,skull and pelvis of the silver fox (V. vulpes)

Directional asymmetry (DA) is a characteristic of most vertebrates, most strikingly exhibited by the placement of various organs (heart, lungs, liver, etc.) but also noted in small differences in the metrics of skeletal structures such as the pelvis of certain fish or sauropsids. We have analyzed DA in the skeleton of the fox (V. vulpes), using ～1,000 radiographs of foxes from populations used in the genetic analysis of behavior and morphology. Careful measurements from this robust data base demonstrate that: 1) DA occurs in the limb bones, the ileum, and ischium and in the mandible; 2) regardless of the direction of the length asymmetry vector of a particular skeletal unit, the vectorial direction of length is always opposite to that of width; 3) with the exception of the humerus and radius, there is no correlation or inverse correlation between vectorial amplitudes or magnitudes of bone asymmetries. 4) Postnatal measurements on foxes demonstrate that the asymmetry increases after birth and continues to change (increasing or decreasing) during postnatal growth. 5) A behavior test for preferential use of a specific forelimb exhibited fluctuating asymmetry but not DA. None of the skeletal asymmetries were significantly correlated with a preferential use of a specific forelimb. We suggest that for the majority of fox skeletal parameters, growth on the right and left side of the fox are differentially biased resulting in fixed differences between the two sides in either the rate of growth or the length of the period during which growth occurs. Random effects around these fixed differences perturb the magnitude of the effects such that the magnitudes of length and width asymmetries are not inversely correlated at the level of individual animals. J. Morphol., 2010. © 2010 Wiley‐Liss, Inc.     

Limits to length asymmetry detection in starlings: implications for biological signalling

Fluctuating asymmetry has received considerable recent attention in evolutionary biology as these small developmental asymmetries can be related to biological fitness and, hence, could be used as a visual cue (or signal) of quality among individuals. The ability of signal receivers to detect and respond to small asymmetries is a fundamental assumption of the symmetry-signalling hypothesis, but has not been experimentally investigated. In this study I have investigated the perceptual threshold to detect and respond to paired-bar length asymmetry in a common bird, the European starling Sturnus vulgaris, by means of operant-learning techniques. The threshold indicates how large the length asymmetry must be to be reliably discriminated from symmetry; birds could not detect an asymmetry of 1.25%. In nature, many asymmetries can be smaller than 1.25%, hence this initial study suggests that caution should be used when trying to invoke symmetry-signalling in natural populations.     

Bilateral variation and the evolutionary origin of macroscopic asymmetries

Given that characters exhibiting macroscopic asymmetry have evolved in a wide variety of taxa, heritable variation for bilateral asymmetry must have arisen at some point in their history. The recognition that heritable variation may underlie some statistical asymmetries not only raises concerns about the incautious use of statistical estimates of FA in studies of developmental stability, but it suggests some intriguing questions about the possible evolutionary origins of macroscopic asymmetries. First, we developed an additive model of bilateral variation based on some simple assumptions about the developmental control of bilateral variation. Second, using a new approach for studying statistical asymmetries, we conducted an analysis of bilateral variation in eight metrical traits of a harpacticoid copepod (Tigriopus californicus) to search for novel forms of statistical asymmetries. The model we developed revealed three independent statistical asymmetries of potential evolutionary significance:a) a previously unrecognized form of asymmetry (referred to here asnormal covariant asymmetry),b) antisymmetry, andc) directional asymmetry. Because each pattern of variation would seem to require different amounts and kinds of developmental-genetic information [a- only negative feedback between sides (bilateral inhibition),b- bothbilateral inhibition and average departure from symmetry (bilateral offset),c- bilateral inhibition, bilateral offset, and a consistent overdevelopment of one side or the other (side-bias control)], those requiring less information would seem more likely to represent earlier stages in the evolution of macroscopic asymmetries. Our analysis of bilateral variation inTigriopus revealed no evidence for any form of statistical asymmetry other than fluctuating asymmetry. However, a significant positive covariation between sides, even after correction for body size variation, suggested that factors influencing relative limb length (whether genetic or environmental) affected both sides equally rather than one side at the expense of the other. Finally, we note that certain statistical asymmetries (directional asymmetry, any form of covariant asymmetry) may render characters unreliable for estimating developmental stability because, unlike pure fluctuating asymmetry, they may signal a genetic component to asymmetry variation.     

Asymmetric neural coding revealed by in vivo calcium imaging in the honey bee brain

Left–right asymmetries are common properties of nervous systems. Although lateralized sensory processing has been well studied, information is lacking about how asymmetries are represented at the level of neural coding. Using in vivo functional imaging, we identified a population-level left–right asymmetry in the honey bee''s primary olfactory centre, the antennal lobe (AL). When both antennae were stimulated via a frontal odour source, the inter-odour distances between neural response patterns were higher in the right than in the left AL. Behavioural data correlated with the brain imaging results: bees with only their right antenna were better in discriminating a target odour in a cross-adaptation paradigm. We hypothesize that the differences in neural odour representations in the two brain sides serve to increase coding capacity by parallel processing.     

Comparison of two kinds of functional asymmetry in the roach <Emphasis Type="Italic">Rutilus rutilus</Emphasis> (Teleostei: Cyprinidae)

In the higher vertebrates, asymmetries of different functions of individual are poorly connected with each other. At present it is unknown whether this poor link is a secondary phenomenon or it is characteristic of different kinds of functional asymmetry already at early stages of vertebrate evolution. In connection with this problem, in the roach Rutilus rutilus was studied asymmetry of two behavioral reactions—movements in an annular corridor and of the C-shape body bending at a sudden action of electrical stimulus. Different individuals prefer a certain direction of movement in the corridor (to the right or to the left). Comparison of these two kinds of asymmetries in the same individuals has shown the absence of significant association between asymmetry of different reactions. The obtained data indicate that already in the lower vertebrates, different kinds of functional asymmetry are controlled by different mechanisms and are poorly associated with each other.     

Eggshell Bacterial Load Is Related to Antimicrobial Properties of Feathers Lining Barn Swallow Nests

The use of feathers to line bird’s nests has traditionally been interpreted as having a thermoregulatory function. Feather-degrading bacteria growing on feathers lining nests may have antimicrobial properties, which may provide an additional benefit to lining nests with feathers. We test the hypothesis that the production of antimicrobial substances by feather bacteria affects the microbiological environment of the nest, and therefore the bacterial density on eggshells and, indirectly, hatching success. These effects would be expected to differ between nests lined with pigmented and white feathers, because bacteria grow differently on feathers of different colors. We experimentally manipulated the composition of pigmented and unpigmented feathers in nests of the barn swallow (Hirundo rustica) and studied the antimicrobial properties against the keratin-degrading bacterium Bacillus licheniformis of bacteria isolated from feathers of each color. Analyzed feathers were collected at the end of the incubation period, and antimicrobial activity was defined as the proportion of bacteria from the feathers that produce antibacterial substances effective against B. licheniformis. Our experimental manipulation affected antimicrobial activity, which was higher in nests with only white feathers at the beginning of incubation. Moreover, white feathers showed higher antimicrobial activity than black ones. Interestingly, antimicrobial activity in feathers of one of the colors correlated negatively with bacterial density on feather of the opposite color. Finally, antimicrobial activity of white feathers was negatively related to eggshell bacterial load. These results suggest that antimicrobial properties of feathers in general and of white feathers in particular affect the bacterial environment in nests. This environment in turn affects the bacterial load on eggshells, which may affect hatching success.     

Comparison of nonlinear models to describe the feather growth and development curve in yellow-feathered chickens

Feathers play a critical role in thermoregulation and directly influence poultry production. Poor feathering adversely affects living appearance and carcass quality, thus reducing profits. However, producers tend to ignore the importance of feather development and do not know the laws of feather growth and development. The objective of this study was to fit growth curves to describe the growth and development of feathers in yellow-feathered broilers during the embryonic and posthatching periods using different nonlinear functions (Gompertz, logistic and Bertalanffy). Feather mass and length were determined during the embryonic development and posthatching stages to identify which growth model most accurately described the feather growth pattern. The results showed that chick embryos began to grow feathers at approximately embryonic (E) day 10, and the feathers grew rapidly from E13 to E17. There was little change from E17 to the day of hatching (DOH). During the embryonic period, the Gompertz function (Y = 798.48e^{−203 431exp(−0.87t)}, Akaike’s information criterion (AIC) = −0.950 × 10³, Bayesian information criterion (BIC) = −0.711 × 10³ and mean square error (MSE) = 559.308) provided the best fit for the feather growth curve compared with the other two functions. After hatching, feather mass and length changed little from the DOH to day (D) 14, increased rapidly from D21 to D91 and then grew slowly after D91. The first stage of feather molting occurred from 2 to 3 weeks of age when the down feathers were mostly shed and replaced with juvenile feathers, and the second stage occurred at approximately 13 to 15 weeks of age. The three nonlinear functions could overall fit the feather growth curve well, but the Bertalanffy model (Y = 116.88 × (1−0.86e^−0.02t)³, AIC = 1.065 × 10⁵, BIC = 1.077 × 10⁵ and MSE = 11.308) showed the highest degree of fit among the models. Therefore, the Gompertz model exhibited the best goodness of fit for the feather growth curve during the embryonic development, while the Bertalanffy model was the most suitable model due to its accurate ability to predict the growth and development of feathers during the growth period, which is an important commercial characteristic of yellow-feathered chickens.     

Cortical asymmetries at different spatial hierarchies relate to phonological processing ability

The ability to map speech sounds to corresponding letters is critical for establishing proficient reading. People vary in this phonological processing ability, which has been hypothesized to result from variation in hemispheric asymmetries within brain regions that support language. A cerebral lateralization hypothesis predicts that more asymmetric brain structures facilitate the development of foundational reading skills like phonological processing. That is, structural asymmetries are predicted to linearly increase with ability. In contrast, a canalization hypothesis predicts that asymmetries constrain behavioral performance within a normal range. That is, structural asymmetries are predicted to quadratically relate to phonological processing, with average phonological processing occurring in people with the most asymmetric structures. These predictions were examined in relatively large samples of children (N = 424) and adults (N = 300), using a topological asymmetry analysis of T1-weighted brain images and a decoding measure of phonological processing. There was limited evidence of structural asymmetry and phonological decoding associations in classic language-related brain regions. However, and in modest support of the cerebral lateralization hypothesis, small to medium effect sizes were observed where phonological decoding accuracy increased with the magnitude of the largest structural asymmetry across left hemisphere cortical regions, but not right hemisphere cortical regions, for both the adult and pediatric samples. In support of the canalization hypothesis, small to medium effect sizes were observed where phonological decoding in the normal range was associated with increased asymmetries in specific cortical regions for both the adult and pediatric samples, which included performance monitoring and motor planning brain regions that contribute to oral and written language functions. Thus, the relevance of each hypothesis to phonological decoding may depend on the scale of brain organization.