Flower Symmetry Preferences in Honeybees and their Crab Spider Predators

Flowers exhibit symmetrical patterns, and innate preferences for symmetry in pollinators like honeybees are documented. Most previous studies of symmetry preferences in honeybees, Apis mellifera, tested levels of asymmetry using artificial flowers or stimuli. Here we investigated the effect of flower asymmetry on flower preferences of honeybees in a novel approach using real flowers, incorporating their spectral properties and how the receivers process the visual signals. Importantly, we also tested the response of an ‘eavesdropping’ predator, the crab spider Thomisus spectabilis, that also utilizes the same flower to prey on honeybees. Flowers (Chrysanthemum frutescens) were manipulated to contain asymmetrical and symmetrical patterns, excluding olfactory cues. Both crab spiders and honeybees exhibited a significant preference for symmetrical flowers. Moreover, honeybees exhibited a significant preference for radial symmetry over bilateral symmetry, but no corresponding effect was recorded in crab spiders. Further analyses demonstrated that flower reflectance and orientation of the axis of symmetry did not affect crab spider decisions. Field observations on T. spectabilis revealed that the natural variation in C. frutescens symmetry had no effect on the choice of crab spiders. This indicates that spiders and honeybees may use other flower characteristics, for example, olfactory cues, together with flower symmetry, to make their foraging decisions.     

Floral symmetry is associated with flower size and pollen production but not insect visitation rates in Geranium robertianum (Geraniaceae)

The degree to which fine‐scaled variation in floral symmetry is associated with variation in plant fitness remains unresolved, as does the question of whether floral symmetry is in itself a target of pollinator‐mediated selection. Geranium robertianum (Geraniaceae) is a broadly distributed species whose five‐petaled flowers vary widely with respect to their degree of rotational asymmetry. In this study, we used a naturally occurring population of plants to investigate whether floral rotational asymmetry and leaf bilateral symmetry were phenotypically correlated with a series of fitness‐related traits, and also used an experimental array with model flowers to investigate the preference of insect visitors for varying degrees of floral size and symmetry. We found that leaf asymmetry was not associated with any of the phenotypic traits measured, and that the degree of floral rotational asymmetry was strongly associated with decreased flower size and decreased pollen production. Our experimental arrays showed that insect visitors did not discriminate among model flowers on the basis of size or symmetry alone; however, insect visitors preferentially visited smaller, symmetric model flowers over larger, severely asymmetric model flowers. Taken together, our results suggest that floral and leaf symmetry in G. robertianum are not likely strong indicators of phenotypic quality, and that floral symmetry is unlikely to be a target of pollinator‐mediated selection. However, the relationship between floral asymmetry and pollen production may provide a role for fecundity selection on symmetry in this species. These data importantly add to the growing literature on the adaptive nature of floral symmetry in the wild.     

Effect of breathing pattern on arm coordination symmetry in front crawl

This study analyzed the relationship between breathing pattern and arm coordination symmetry in 11 expert male swimmers who performed the front crawl at their 100-m race pace using seven randomized breathing patterns. Two indexes of coordination (IdCP and IdCNP) and a symmetry index (SI) based on the difference of IdCP - IdCNP were calculated. IdCP calculated the lag time between the beginning of arm propulsion on the nonpreferential breathing side and the end of arm propulsion on the preferential breathing side; IdCNP did the converse. The IdCP and IdCNP comparisons and the SI showed coordination asymmetries among the seven breathing patterns. Specifically, breathing to the preferential side led to an asymmetry, in contrast to the other breathing patterns, and the asymmetry was even greater when the swimmer breathed to his nonpreferential side. These findings highlight the effect of breathing laterality in that coordination was symmetric in patterns with breathing that was bilateral, axed (as in breathing with a frontal snorkel), or removed (as in apnea). One practical application is that arm coordination asymmetry can be prevented or reduced by using breathing patterns that balance the coordination.     

Fluctuating asymmetry in red junglefowl

Fluctuating asymmetry, the random deviation from perfect bilateral symmetry, has recently attracted considerable attention. Levels of asymmetry have been shown to correlate with measures of individual quality. We measured asymmetry in a variety of ornamental and non-ornamental traits in red junglefowl, Gallus gallus and examined the patterns of asymmetry among different traits within an individual. All ornamental traits had significantly higher levels of fluctuating asymmetry than did non-ornamental traits. However, inter-trait correlations of asymmetry were low for both ornamental and non-ornamental traits. We then correlated measures of asymmetry with several potential indicators of male quality, including comb size, body size, and body condition. We found little evidence that asymmetry in any measured trait reflected male quality. We measured asymmetry in ornamental traits at several stages of development and found no relationship between male condition and changes in asymmetry over time. Our results indicate that it is necessary to employ caution when choosing traits to be measured in studies of fluctuating asymmetry and that a relationship between asymmetry and individual quality cannot be assumed.     

Regulation of midline development by antagonism of lefty and nodal signaling.

The embryonic midline is crucial for the development of embryonic pattern including bilateral symmetry and left-right asymmetry. In zebrafish, lefty1 (lft1) and lefty2 (lft2) have distinct midline expression domains along the anteroposterior axis that overlap with the expression patterns of the nodal-related genes cyclops and squint. Altered expression patterns of lft1 and lft2 in zebrafish mutants that affect midline development suggests different upstream pathways regulate each expression domain. Ectopic expression analysis demonstrates that a balance of lefty and cyclops signaling is required for normal mesendoderm patterning and goosecoid, no tail and pitx2 expression. In late somite-stage embryos, lft1 and lft2 are expressed asymmetrically in the left diencephalon and left lateral plate respectively, suggesting an additional role in laterality development. A model is proposed by which the vertebrate midline, and thus bilateral symmetry, is established and maintained by antagonistic interactions among co-expressed members of the lefty and nodal subfamilies of TGF-beta signaling molecules.     

Roles of Type I Myosins in Drosophila Handedness

Although bilateral animals, including Drosophila, appear to have left-right (LR) symmetry from the outside, their internal organs often show directional and stereotypical LR asymmetry. The mechanisms by which the LR axis is established in Drosophila have not been studied well. We showed that two type I Myosin proteins play crucial roles in the manifestation of Drosophila handedness. Mutants of Myosin31DF (Myo31DF), which encodes a type ID Myosin, showed reversed laterality of the embryonic and adult gut and testis. Myo31DF was required in the epithelial cells of the embryonic hindgut, where its protein co-localized with actin filaments, for the correct handedness of this organ. Disorganization of the actin cytoskeleton in the hindgut epithelium caused LR defects of the embryonic hindgut. These results suggest that the actin-based Myo31DF function is required for proper handedness. In contrast, the disruption of microtubules in the hindgut epithelium did not affect the laterality of this organ. We also found that the overexpression of Myosin61F (Myo61F), which encodes another type I Myosin, in the hindgut epithelium reversed the hindgut handedness, suggesting that these two type I Myosins, Myo31DF and Myo61F, have antagonistic functions. We propose that the actin-based functions of type I Myosins play critical roles in generating LR asymmetry in invertebrates.     

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.     

Sex determination and optimal development in the Moorish gecko,Tarentola mauritanica

Under temperature sex determination (TSD), sex is determined by temperature during embryonic development. Depending on ecological and physiological traits and plasticity, TSD species may face demographic collapse due to climate change. In this context, asymmetry in bilateral organisms can be used as a proxy for developmental instability and, therefore, deviations from optimal incubation conditions. Using Tarentola mauritanica gecko as a model, this study aimed first to confirm TSD, its pattern and pivotal temperature, and second to assess the local adaptation of TSD and variation of asymmetry patterns across four populations under different thermal regimes. Eggs were incubated at different temperatures, and hatchlings were sexed and measured. The number of lamellae was counted in adults and hatchlings. Results were compatible with a TSD pattern with males generated at low and females at high incubation temperatures. Estimated pivotal temperature coincided with the temperature producing lower embryonic mortality, evidencing selection towards balanced sex ratios. The temperature of oviposition was conservatively selected by gravid females. Asymmetry patterns found were likely related to nest temperature fluctuations. Overall, the rigidity of TSD may compromise reproductive success, and demographic stability in this species in case thermal nest choice becomes constrained by climate change.     

Time,pattern, and heterochrony: a study of hyperphalangy in the dolphin embryo flipper

The forelimb of whales and dolphins is a flipper that shows hyperphalangy (numerous finger bones). Hyperphalangy is also present in marine reptiles, including ichthyosaurs and plesiosaurs. The developmental basis of hyper-phalangy is unclear. Kükenthal suggested that phalanx anlagen split into three pieces during cetacean development, thereby multiplying the ancestral number. Alternatively, Holder suggested that apical ectodermal ridge (AER)-directed limb outgrowth might be prolonged by a timing shift (heterochrony), leading to terminal addition of extra phalanges. We prepared a series of whole mounted and serially sectioned embryonic flipper buds of the spotted dolphin Stenella attenuata. This cetacean shows marked hyperphalangy on digits II and III. We confirm previous reports that the proximodistal laying down of phalanges is prolonged in digits II and III. Histology showed that the apical ectoderm was thickened into a cap. There was a weak ridge-like structure in some embryos. The cap or ridge formed part of a bud-like mass that persisted on digits II and III at stages when it had disappeared from other digits. Thus the dolphin differs from other mammals in showing a second period of limb outgrowth during which localized hyperphalangy develops. New phalanges only formed at the tip of the digits. These findings are consistent with a model in which heterochrony leads to the terminal addition of new phalanges. Our results are more easily reconciled with the progress zone model than one in which the AER is involved in the expansion of a prepattern. We suggest that patterning mechanisms with a temporal component (i.e., the "progress zone" mechanism) are potential targets for heterochrony during limb evolution.     

Parasites increase fluctuating asymmetry of maleDrosophila nigrospiracula: Implications for sexual selection

Fluctuating asymmetry (minor deviations from perfect bilateral symmetry) is manifested by individuals less able to buffer environmental stress during development. I utilized a system of two naturally-occurring parasites ofDrosophila nigrospiracula to test whether parasitic infection during host development yields elevated degrees of fluctuating asymmetry in two morphological traits of males. This hypothesis has important implications for sexual selection, as it may explain why asymmetric males are often found to be sexually disadvantaged. In my system, nematodes infect larvae and therefore are more likely to disrupt development than mites which only parasitize adult flies. As predicted, nematode-infected maleD. nigrospiracula had a higher degree of bristle asymmetry than did mite-infested and control (carrying neither parasite) males. There was also a significant relation between nematode number and degree of asymmetry. There was a significant negative relation between nematode load and size of adult males, implicating a causal link between nutritional stress during host development and fluctuating asymmetry. Patterns of wing length asymmetry were inconsistent with those of bristle asymmetry. Nematode-infected males did not differ in wing length asymmetry relative to mite-infested and control males, nor was there a significant relation between nematode number and wing asymmetry. This inconsistency in expression of asymmetry may reflect different intensities of selection operating on each morphological trait.     

A jumping spider that lays eggs like an insect

The South East Asian salticid, Asemonea tenuipes, lay its eggs like an insect: as individuated capsules in geometrically precise rows. The occurrence of this behaviour is described in a population from Thailand that lays eggs on the underside of mango tree (Mangifera indica) leaves. The rows were vertically arranged at a 90° angle that was parallel to, and varied in relation to the angle of the central leaf rib, indicating that the rib serves as the primary visual cue for orienting the row. Analysis of within-egg row symmetry found evidence that micro-topography – in particular, vertical ‘stepping’ produced by leaf sub-ribs – of the leaf surface plane was responsible for 97% of variability in the relative symmetry of egg placement. Three strategies were identified: (1) crossing the sub-rib and producing localized asymmetry in the egg row; (2) introducing a gap at the sub-rib to maintain symmetry; and (3) ‘compressing’ the egg row into the gap between sub-ribs. The incidence of asymmetry showed a highly significant linear relationship with egg load. It is hypothesized that the use of rows probably represents a solution to the problem of how to surveil temporally staggered clutches of eggs and newly hatched spiderlings simultaneously.     

A method for quantifying rotational symmetry

Here, a new approach for quantifying rotational symmetry based on vector analysis was described and compared with information obtained from a geometric morphometric analysis and a technique based on distance alone. A new method was developed that generates a polygon from the length and angle data of a structure and then quantifies the minimum change necessary to convert that polygon into a regular polygon. This technique yielded an asymmetry score (s) that can range from 0 (perfect symmetry) to 1 (complete asymmetry). Using digital images of Geranium robertianum flowers, this new method was compared with a technique based on lengths alone and with established geometric morphometric methods used to quantify shape variation. Asymmetry scores (s) more clearly described variation in symmetry and were more consistent with a visual assessment of the images than either comparative technique. This procedure is the first to quantify the asymmetry of radial structures accurately, uses easily obtainable measures to calculate the asymmetry score and allows comparisons among individuals and species, even when the comparisons involve structures with different patterns of symmetry. This technique enables the rigorous analysis of polysymmetric structures and provides a foundation for a better understanding of symmetry in nature.     

Fearful symmetry? Intra-individual comparisons of asymmetry in cryptic vs. signalling colour patterns in butterflies

The signalling role of asymmetry has attracted considerable recent interest among evolutionary biologists. Although it has been studied primarily within the context of sexual selection, symmetry of signals may play a role also in inter-specific communication, such as predator–prey interactions. Both theory and experimental evidence suggest that asymmetry may impair the efficacy of visual warning signals used to deter potential predators, but increase the protective value of non-signalling, cryptic colour patterns used to decrease the risk of detection. Here we tested the prediction from this hypothesis by means of intra-individual comparisons of asymmetry in colour pattern elements in three species of moths (Arctia caja (L.), Noctua orbona (L.), Smerinthus ocellata (L.)) that possess cryptic fore wing patterns and signalling hind wing patterns. Mean asymmetries constituted 4.3% (range 2.1–7.0%) of trait size for colour pattern elements, whereas individual asymmetry levels reached as high as 26%. Asymmetry tended to be somewhat larger in cryptic patterns on fore wings than in signalling patterns on hind wings in five of six comparisons, but in only one case was the difference statistically significant. In addition, pattern elements were somewhat more asymmetric on fore wings also in Saturnia pavonia (L.), which possesses identical signalling eyespots on both fore and hind wings. The relatively low levels of asymmetry also in cryptic patterns imply either that selection does not favour increased asymmetry in cryptic patterns, or that the evolution of pronounced asymmetry is developmentally or genetically constrained.     

Strategies to establish left/right asymmetry in vertebrates and invertebrates

Left/right (L/R) asymmetry is essential during embryonic development for organ positioning, looping and handed morphogenesis. A major goal in the field is to understand how embryos initially determine their left and right hand sides, a process known as symmetry breaking. A number of recent studies on several vertebrate and invertebrate model organisms have provided a more complex view on how L/R asymmetry is established, revealing an apparent partition between deuterostomes and protostomes. In deuterostomes, nodal cilia represent a conserved symmetry-breaking process; nevertheless, growing evidence shows the existence of pre-cilia L/R asymmetries involving active ion flows. In protostomes like snails and Drosophila, symmetry breaking relies on different mechanisms, involving, in particular, the actin cytoskeleton and associated molecular motors.     

Perfect is best: low leaf fluctuating asymmetry reduces herbivory by leaf miners

Fluctuating asymmetry (FA) represents small, random variation from symmetry and can be used as an indicator of plant susceptibility to herbivory. We investigated the effects of FA of two oak species, Quercus laevis and Q. geminata, and the responses of three herbivore guilds: leaf miners, gallers, and chewers. To examine differences in FA and herbivory between individuals, 40 leaves from each tree were collected, and FA indices were calculated. To examine differences in FA and herbivory within-individuals, we sampled pairs of mined and unmined leaves for asymmetry measurements. Differences in growth of leaf miners between leaf types were determined by tracing 50 mines of each species on symmetric leaves and asymmetric leaves. Asymmetric leaves contained significantly lower concentrations of tannins and higher concentrations of nitrogen than symmetric leaves for both plant species. Both frequency of asymmetric leaves on plants and levels of asymmetry positively influenced the abundance of Brachys, Stilbosis and other leaf miners, but no significant relationship between asymmetry and herbivory was observed for Acrocercops. Brachys and Stilbosis mines were smaller on asymmetric leaves, but differences in mine survivorship between symmetric and asymmetric leaves were observed only for Stilbosis mines. This study indicated that leaf miners might use leaf FA as a cue to plant quality, although differential survivorship among leaf types was not observed for all species studied. Reasons for the different results between guilds are discussed.     

Phalangeal morphology of the Paromomyidae (?Primates,Plesiadapiformes): The evidence for gliding behavior reconsidered

A comparative morphometric analysis of isolated proximal and intermediate phalanges attributed to the paromomyids Ignacius graybullianus and Phenacolemur simonsi was undertaken to test the hypothesis that these fossil phalanges exhibit evidence of a dermopteran-like interdigital patagium. Linear dimensions were collected for the fossil phalanges and a comparative sample of associated proximal and intermediate phalanges representing extant tree squirrels, tree shrews, dermopterans (colugos), gliding rodents and marsupials, and prosimian primates. Quantitative data indicate that the proximal and intermediate phalanges of paromomyids are most similar in their overall shape to those of the dermopteran Cynocephalus. The proximal phalanges of paromomyids and colugos possess well-developed flexor sheath ridges and broad, high shafts, whereas the intermediate phalanges of these taxa are most similar to one another in their trochlear morphology. Discriminant analysis indicates that all of the paromomyid intermediate phalanges resemble those from colugo toes more so than those from colugo fingers. Moreover, the relative length and midshaft proportions of both the proximal and intermediate phalanges of paromomyids closely resemble those of several squirrels that lack an interdigital patagium. The following conclusions are drawn from this study: 1) paromomyids share a number of derived phalangeal features with modern dermopterans that may be indicative of a phylogenetic relationship between them, 2) existing intermediate phalanges of paromomyids are inconsistent with the “mitten gliding” hypothesis because they do not possess the distinctive length and midshaft proportions characteristic of colugo manual intermediate phalanges, and 3) paromomyids share with colugos and the scaly-tailed squirrel Anomalurus several aspects of phalangeal morphology functionally related to frequent vertical clinging and climbing on large-diameter arboreal supports. Am J Phys Anthropol 109:397–413, 1999. © 1999 Wiley-Liss, Inc.     

Patterns of fluctuating asymmetry in the limbs of freshwater turtles: Are more functionally important limbs more symmetrical?

Understanding how selective forces influence patterns of symmetry remains an active area of research in evolutionary biology. One hypothesis, which has received relatively little attention, suggests that the functional importance of morphological characters may influence patterns of symmetry. Specifically, it posits that for structures that display bilateral symmetry, those with greater functional importance should display lower levels of asymmetry. The aim of this study was to examine the patterns of fluctuating asymmetry (FA) present in the limb bones of freshwater turtles in the family Emydidae. Aquatic emydid turtles of the subfamily Deirochelyinae employ a hindlimb-dominant swimming style, suggesting that hindlimbs should display lower levels of FA. Consistent with the morpho-functional hypothesis of symmetry, we found a strong, clade-wise pattern of humeral-biased FA in aquatic Deirochelyinae. In contrast, some emydids of the subfamily Emydinae possess more terrestrial tendencies. As terrestrial locomotion places more equal importance on fore- and hindlimbs, we predicted that such behaviors may minimize differences in FA. No clade-wise pattern was detected in the subfamily Emydinae. We also detected a phylogenetic signal in FA within the femur and discovered that FA has evolved at vastly different rates between the fore- and hindlimbs.     

Great tits (Parus major) searching for artificial prey: implications for cryptic coloration and symmetry

It has been suggested that bilateral symmetry may impose a costfor animals relying on camouflage because symmetric color patternsmight increase the risk of detection. We tested the effect ofsymmetry on crypsis, carrying out a predation experiment withgreat tits (Parus major) and black-and-white–patterned,artificial prey items and background. First, we found that detectiontime was significantly longer for a highly cryptic, asymmetricpattern based on a random sample of the background than forits symmetric variants. Second, we were able to arrange theelements of a prey pattern in a way that the resulting asymmetricpattern was highly cryptic and, furthermore, its symmetric variantwas highly cryptic as well. We conclude that symmetry may imposea substantial cost on cryptic patterns, but this cost variesamong patterns. This suggests that for prey, which predatorstypically view from an angle exposing their symmetry, selectionfor pattern asymmetry may be less important and selection fordecreased detectability cost of symmetry may be more importantthan previously thought. This may help to understand the existenceof so many prey with cryptic, symmetric color patterns.     

Comment on feedback training of parietal-occipital alpha asymmetry in normal human subjects

Experiments with feedback regulation of normal subjects' parietal-occipital alpha electroencephalographic asymmetry have shown that subjects learned to optimize the conditions under which symmetry and asymmetry occurred. Asymmetry was defined as the difference in the occurrence of the two hemispheres' alpha EEG activity. The results of this experiment can be interpreted to mean that the subjects did not learn alpha asymmetry per se, but instead learned to increase then percent time of alpha and increase the alternations between alpha and no alpha. This condition is optimized when the subject has his eyes closed and is not performing a visual search. On the other hand, symmetry is optimized when the subject performs a visual task. Methodological problems in feedback training are discussed.