Visual signalling by asymmetry: a review of perceptual processes.

Individual levels of asymmetry in traits that display fluctuating asymmetry could be used as visual signals of phenotypic (and perhaps genotypic) quality, as asymmetry can often be negatively related to fitness parameters. There are some data to support this hypothesis but the experimental protocols employed have commonly resulted in asymmetries far larger than those observed in nature. To date, there has been little consideration of the ability of animals to accurately discriminate small asymmetries (of the magnitude observed in the wild) from perfect symmetry. This is key to assessing the plausibility of the asymmetry-signalling hypothesis. Here, I review the perceptual processes that may lead to the discrimination of asymmetry and discuss a number of ecologically relevant factors that may influence asymmetry signalling. These include: signal orientation, distance of trait elements from the axis of symmetry, trait complexity, trait contrast and colour, and the behaviour of both signaller and receiver. I also discuss the evolution of symmetry preferences and make suggestions as to where researchers should focus attention to examine the generality of asymmetry-signalling theory. In highly developmentally stable signalling systems the magnitude of asymmetry may be too small to be detected accurately and reliably, hence asymmetry signalling is unlikely to have evolved in these situations.     

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.     

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.     

Courtship and genetic quality: asymmetric males show their best side

Fluctuating asymmetry (FA), the small random deviations from perfect morphological symmetry that result during development, is ubiquitous throughout the animal kingdom. In many species, FA seems to play a role in mate choice, perhaps because it signals an individual''s genetic quality and health. However, the relationship between an individual''s FA and behaviour is generally unknown: what do more asymmetric individuals do about their own asymmetry? We now show for the first time that individuals respond behaviourally to their own morphological FA in what appears to be an adaptive manner. During courtship, male guppies exhibiting high FA in ornamental colour, bias their displays towards their more colourful body side, thus potentially increasing their attractiveness by exaggerating the quantity of their orange signal. This appears to be a strictly behavioural male response to cues provided by females, as it does not occur when males court a non-reactive model female. Whether inferior males realize any mating advantage remains uncertain, but our study clearly demonstrates a behavioural response to random morphological asymmetries that appears to be adaptive. We propose that the tendency to show or otherwise use a ‘best side’ is common in nature, with implications for sexual signalling and the evolution of more pronounced asymmetries.     

Persistence of subtle departures from symmetry over multiple molts in individual brachyuran crabs: Relevance to developmental stability

Fluctuating asymmetry (FA) is generally viewed as a population-level character. It is described by some measure of the variance of the difference between the right and left sides for a collection of individuals. Very little is known of the developmental origins of FA, despite the fact that FA is widely used to estimatedevelopmental stability. We present a novel technique for examining the growth trajectory of the asymmetries that give rise to FA, and we explore two sample data sets for the brachyuran crabHemigrapsus nudus. We have traced the fate of these small, random deviations from perfect symmetry through three successive molts of individual crabs. Invertebrates that molt, and hence grow in discrete steps, provide an easily preserved record of their growth. Model II regressions of measurements from one molt versus the previous molt can help describe the stability of subtle departures from symmetry over time. Although any number of different patterns may occur, we identify four general cases: a) asymmetries vary at random throughout growth (random determination), b) asymmetries remain unchanged in sign and magnitude (constant asymmetries), c) asymmetries increase in proportion to character size and hence increase with growth (size-dependent asymmetries), and d) asymmetries persist, but are reduced in magnitude (damped asymmetries). Data from tenHemigrapsus nudus, measured for between 21 and 28 metrical, limb-segment characters over three successive molts, yielded associations most similar to our pattern ‘b’, although some subtle departures in the direction of pattern ‘c’ were also observed. Persistent asymmetries accounted for 26% and 20% of the variance among asymmetries between molts 1 and 2, and molts 2 and 3 respectively. Thus, in spite of large and rapid increments in the external size of the crab, these subtle asymmetries tended to persist in both direction and magnitude, from molt to molt. This result suggests either i) that individual crabs have a genetic predisposition towards asymmetry in a particular direction but contribute to a continuous and normal distribution ofR-L differences at the population level, or ii) that these subtle asymmetries arose at some earlier ontogenetic stage and were preserved through growth. Either interpretation has important ramifications for the study of FA. The first suggests that under some circumstances FA may not provide a valid measure of developmental instability, because subtle departures from symmetry in an individual may have a genetic basis. The second implies that subtle departures from bilateral symmetry are not ‘corrected’ as an individual grows.     

Cryptic asymmetry: unreliable signals mask asymmetric performance of crayfish weapons

Animals commonly use their limbs as signals and weapons during territorial aggression. Asymmetries of limb performance that do not relate to asymmetries of limb size (cryptic asymmetry) could substantially affect disputes, but this phenomenon has not been considered beyond primates. We investigated cryptic asymmetry in male crayfish (Cherax dispar), which commonly use unreliable signals of strength during aggression. Although the strength of a chela can vary by an order of magnitude for a given size, we found repeatable asymmetries of strength that were only weakly related to asymmetries of size. Size-adjusted strength of chelae and the asymmetry of strength between chelae were highly repeatable between environmental conditions, suggesting that asymmetries of strength stemmed from variation in capacity rather than motivation. Cryptic asymmetry adds another dimension of uncertainty during conflict between animals, which could influence the evolution of unreliable signals and morphological asymmetry.     

Starlings can categorize symmetry differences in dot displays

Fluctuating asymmetry is an estimate of developmental stability and, in some cases, the asymmetry of morphological traits can reflect aspects of individual fitness. As asymmetry can be a marker for fitness, it has been proposed that organisms could use morphological asymmetry as a direct visual cue during inter- and intraspecific encounters. Despite some experimental evidence to support this prediction, the perceptual abilities of animals to detect and respond to symmetry differences have been largely overlooked. Studying the ability of animals to perceive symmetry and factors that affect this ability are crucial to assessing whether fluctuating asymmetry could be used as a visual cue in nature. In this study, we investigated the ability of wild-caught European starlings Sturnus vulgaris to learn to discriminate symmetry from asymmetry in random dot patterns through operant learning experiments. The birds did not possess a spontaneous preference for either symmetry or asymmetry. The birds learned a symmetry preference, although the learning process took longer than that previously reported for pigeons Columba livia and was more error prone. After being trained to discriminate symmetry differences in random dot patterns, birds successfully transferred their symmetry discrimination abilities to a set of novel stimuli that they had not previously seen. This indicates that starlings can form a mental categorization of visual stimuli on the basis of a somewhat generalized symmetry phenomenon. We discuss these findings in relation to the probability that birds use fluctuating asymmetry as a visual cue.     

Asymmetry in Signal Propagation between the Soma and Dendrites Plays a Key Role in Determining Dendritic Excitability in Motoneurons

It is widely recognized that propagation of electrophysiological signals between the soma and dendrites of neurons differs depending on direction, i.e. it is asymmetric. How this asymmetry influences the activation of voltage-gated dendritic channels, and consequent neuronal behavior, remains unclear. Based on the analysis of asymmetry in several types of motoneurons, we extended our previous methodology for reducing a fully reconstructed motoneuron model to a two-compartment representation that preserved asymmetric signal propagation. The reduced models accurately replicated the dendritic excitability and the dynamics of the anatomical model involving a persistent inward current (PIC) dispersed over the dendrites. The relationship between asymmetric signal propagation and dendritic excitability was investigated using the reduced models while varying the asymmetry in signal propagation between the soma and the dendrite with PIC density constant. We found that increases in signal attenuation from soma to dendrites increased the activation threshold of a PIC (hypo-excitability), whereas increases in signal attenuation from dendrites to soma decreased the activation threshold of a PIC (hyper-excitability). These effects were so strong that reversing the asymmetry in the soma-to-dendrite vs. dendrite-to-soma attenuation, reversed the correlation between PIC threshold and distance of this current source from the soma. We propose the tight relation of the asymmetric signal propagation to the input resistance in the dendrites as a mechanism underlying the influence of the asymmetric signal propagation on the dendritic excitability. All these results emphasize the importance of maintaining the physiological asymmetry in dendritic signaling not only for normal function of the cells but also for biophysically realistic simulations of dendritic excitability.     

Fitness disadvantages to disrupted embryogenesis impose selection against suboptimal nest-site choice by female grass snakes, Natrix natrix (Colubridae)

Phenotypic traits of hatchling reptiles are strongly influenced by incubation regimes (e.g. of temperature and moisture), suggesting that maternal choice of suitable nest-sites should be under intense selection. Our laboratory incubation of 209 eggs (17 clutches) from wild-caught Swedish grass snakes (Natrix natrix) showed that scale abnormalities (half-scales on one side of the body, often reflecting lateral asymmetry in the number of ribs) occurred more frequently if eggs were incubated under cooler conditions. Especially at low incubation temperatures, individuals with scale asymmetries took longer to hatch than did symmetric conspecifics, were smaller in body length at hatching and were slower in trials of locomotor speed. Anti-predator tactics also covaried with scale asymmetry. These patterns suggest that individuals with asymmetric scales should have lower fitness and hence should rarely survive to adulthood in the wild. We tested this prediction by examining 201 field-collected snakes from museum collections. As predicted, scale asymmetries were seen primarily in small snakes, and rarely in larger animals. We interpret these data to suggest that scale asymmetries in this species offer an index of developmental instability and that fitness disadvantages to disrupted embryogenesis impose selection against suboptimal nest-site choice by females.     

How Useful is Fluctuating Asymmetry in Conservation Biology: Asymmetry in Rare and Abundant Coenonympha Butterflies

It has been suggested that minor, fluctuating differences in size of bilateral traits could validly indicate individual differences in developmental stability. One plausible reason for instability to occur could be lowered population size, which has been suggested to increase fluctuating asymmetry due to inbreeding, for example. We measured seven wing asymmetries of three Coenonympha butterfly species in central Sweden. One species is abundant (nobreak C. pamphilus), one rather common (C. arcania), and one rare (C. hero). We expected that if fluctuating asymmetry is a reliable indicator of population quality and thus a useful tool for conservation purposes, the most abundant species should show lowest asymmetry and the most endangered, the highest. Contrary to our expectations, the highest wing asymmetry was found in the relatively common species C. arcania and the most abundant and rare species did not show significant differences in levels of wing asymmetry. Our results obtained from three Coenonympha species hence suggest that the use of fluctuating asymmetry as an indicator of population conservation status may be misleading. Possible increase in asymmetry of small and/or isolated populations of butterflies may be masked by local differences in environmental conditions that could have high impact on bilateral development as well.     

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.     

Fluctuating Asymmetry in Menidia beryllina before and after the 2010 Deepwater Horizon Oil Spill

Assessing the impacts of the Deepwater Horizon oil spill with a dependable baseline comparison can provide reliable insight into environmental stressors on organisms that were potentially affected by the spill. Fluctuating asymmetry (small, non-random deviations from perfect bilateral symmetry) is an informative metric sensitive to contaminants that can be used to assess environmental stress levels. For this study, the well-studied and common Gulf of Mexico estuarine fish, Menidia beryllina, was used with pre and post-oil spill collections. Comparisons of fluctuating asymmetry in three traits (eye diameter, pectoral fin length, and pelvic fin length) were made pre and post-oil spill across two sites (Old Fort Bayou and the Pascagoula River), as well as between years of collection (2011, 2012)-one and two years, respectfully, after the spill in 2010. We hypothesized that fluctuating asymmetry would be higher in post-Deepwater Horizon samples, and that this will be replicated in both study areas along the Mississippi Gulf coast. We also predicted that fluctuating asymmetry would decrease through time after the oil spill as the oil decomposed and/or was removed. Analyses performed on 1135 fish (220 pre and 915 post Deepwater Horizon) showed significantly higher post spill fluctuating asymmetry in the eye but no difference for the pectoral or pelvic fins. There was also higher fluctuating asymmetry in one of the two sites both pre and post-spill, indicating observed asymmetry may be the product of multiple stressors. Fluctuating asymmetry decreased in 2012 compared to 2011. Fluctuating asymmetry is a sensitive measure of sub lethal stress, and the observed variability in this study (pre vs. post-spill or between sites) could be due to a combination of oil, dispersants, or other unknown stressors.     

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.     

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.     

Spike-Threshold Adaptation Predicted by Membrane Potential Dynamics In Vivo

Neurons encode information in sequences of spikes, which are triggered when their membrane potential crosses a threshold. In vivo, the spiking threshold displays large variability suggesting that threshold dynamics have a profound influence on how the combined input of a neuron is encoded in the spiking. Threshold variability could be explained by adaptation to the membrane potential. However, it could also be the case that most threshold variability reflects noise and processes other than threshold adaptation. Here, we investigated threshold variation in auditory neurons responses recorded in vivo in barn owls. We found that spike threshold is quantitatively predicted by a model in which the threshold adapts, tracking the membrane potential at a short timescale. As a result, in these neurons, slow voltage fluctuations do not contribute to spiking because they are filtered by threshold adaptation. More importantly, these neurons can only respond to input spikes arriving together on a millisecond timescale. These results demonstrate that fast adaptation to the membrane potential captures spike threshold variability in vivo.     

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.     

On the adaptive accuracy of directional asymmetry in insect wing size

Subtle left-right biases are often observed in organisms with an overall bilateral symmetry. The evolutionary significance of these directional asymmetries remains uncertain, however, and scenarios of both developmental constraints and adaptation have been suggested. Reviewing the literature on asymmetry in insect wings, we analyze patterns of directional asymmetry in wing size to evaluate the possible adaptive significance of this character. We found that directional asymmetry in wing size is widespread among insects, with left- and right-biased asymmetries commonly observed. The direction of the asymmetry does not appear to be evolutionarily conserved above the species level. Overall, we argue that the very small magnitude of directional asymmetry, 0.7% of the wing size on average, associated with an extremely imprecise expression, precludes directional asymmetry from playing any major adaptive role.     

Does fluctuating asymmetry of antlers in white-tailed deer (Odocoileus virginianus) follow patterns predicted for sexually selected traits?

Secondary sexual characters have been hypothesized to signal male quality and should demonstrate a negative relationship between the size of the trait and degree of fluctuating asymmetry because they are costly to produce. We collected morphometric and antler data from 439 white-tailed deer (Odocoileus virginianus) in Oklahoma, USA, in order to determine whether measures of antler asymmetry follow the patterns predicted for sexually selected characters. Relative fluctuating asymmetry was negatively related to antler size for all deer and within age groups up to five and a half years of age. We did not detect an association between asymmetry and antler size among deer that were six and a half years or older. When categorizing deer by antler size, we found that deer with small antlers (< or = 33rd percentile) had greater levels of relative asymmetry than deer with large antlers (< or = 67th percentile). The relative asymmetry of antlers was negatively related to age and was greatest in deer that were one and a half years old. Relative asymmetry was also negatively related to carcass mass, inside spread, skull length and body length. These data suggest that asymmetry in the antlers of white-tailed deer may be a reliable signal of quality and, as such, may be important in maintaining honesty in intrasexual advertisements during the breeding season.     

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.