Female preference for the pheromone of males with low fluctuating asymmetry in the Japanese scorpionfly (Panorpa japonica: Mecoptera)

Fluctuating asymmetry (FA) is denned as small, random deviationsfrom perfect bilateral symmetry in a bilaterally symmetricalmorphological trait. The relationship between FA in forewinglength of males and the relative sexual attractiveness of theirpair-formation pheromones was studied experimentally in theJapanese scorpionfly, Panorpa japonica. This is the first studyof the role of FA in pheromonal communication systems, and oneof only a few studies on the relationship between FA and sexualselection. Collectively, the results of four interrelated experimentsreveal that females prefer the pheromone of males of relativelylow FA in forewing length. The experimental manipulation offorewing FA of males by cutting wing lengths did not influencetheir olfactory attractiveness to females. In this case, femaleschose the male with the lowest premanipulation FA. Thus, naturalwing length FA apparently is correlated with inherent differencesbetween males that influence the properties of sex attractantmales produce. Female preference for low-FA males may be adaptiveas a result of material and/or genetic benefits received byfemales.     

Dimorphisms and fluctuating asymmetry in the forceps of male earwigs

Male dimorphisms are particularly conspicuous examples of the alternative reproductive strategies employed within some species. Such dimorphisms are thought to exist as genetic polymorphisms under ESS conditions, or to be conditional strategies where exogenous conditions determine the adult body plan. Fluctuating asymmetry (FA) is currently considered to be a fitness correlate of significant use in interpreting the functional significance of secondary sexual characteristics. In particular, negative slopes of FA on trait size are thought to arise in traits whose expression is dependent on condition. We measured forceps lengths and asymmetries in 2 island populations of the European earwig Forficula auricularia and Museum specimens of 5 other earwig (Dermaptera, Forficulidae) species from different genera, that appeared to be dimorphic. In a detailed study of Forficula auricularia we found a significant fit to a statistical model for the identification of dimorphisms and, for all species examined, morphs differed in the slope and/or elevation of the allometric relationship between body size and forcep length. Possible determinates of male dimorphisms are suggested from the data. Contrary to expectation, FA was not found to be greater in the minor morphs. Negative relationships between FA and forceps length were absent in both morphs of species examined from museum collections. Of the two island populations of Forficula auricularia, the smaller and more isolated population had higher FA and a negative relationship between FA and forceps length in the major morph. We discuss these patterns in the light of recent theories of FA and honest signalling.     

Relationship between exposure to an insecticide and fluctuating asymmetry in a damselfly (Odonata,Coenagriidae)

In this study, we explored the effects of pesticide on fluctuating asymmetry (FA) levels and mortality of Ceriagrion sp. larvae. The results showed that the mortality of larval damselflies treated with pesticide was significantly higher than that treated with tap water which had been aerated for 48 h, but there were no significant differences among mortality of larvae treated with different concentrations of pesticide. Meanwhile, we found that the level of FA of the first tibia length, one of the seven bilaterally symmetrical traits (First femur length, First tibia length, Second femur length, Second tibia length, Third femur length, Third tibia length and Prementum width), differed significantly with different treatments, whereas the others did not show any significant differences. The Bonferroni (Dunn) t Tests revealed that FA of the first tibia length at 15 × 10⁻⁹ mgl⁻¹ was significantly higher than that at 1.5 × 10⁻⁹ mgl⁻¹ and control. There was no significant relationship between trait size and the absolute difference between their right and left sides. There was also no significant relationship between body size and the absolute difference between right and left sides. Trait size was significantly positively correlated with body size. FA was not associated with mortality. Therefore, we concluded that FA of the first tibia length of Ceriagrion sp. larvae may be induced by sublethal doses of pesticides. That is to say, its FA may be regarded as an indicator of reflecting the level of pesticide stress. Handling editor: K. Martens     

Patterns of fluctuating asymmetry in the limbs of anurans

It has been hypothesized that fluctuating asymmetry (FA) may provide an indication of the functional importance of structures within an organism, with structures that more strongly impact fitness being more symmetric. Based on this idea, we predicted that for tetrapods in which the forelimbs and hindlimbs play an unequal role in locomotion, the less functionally important limb set should display higher levels of FA. We conducted a multispecies test of this hypothesis in anurans (frogs and toads), whose saltatory locomotor mode is powered by the hindlimbs. We also tested whether FA in the forelimbs, which play a more important role during landing, differed between families that differ in the degree of forelimb use in locomotion (Bufonidae vs. Ranidae). We calculated FA from the lengths of humeri and femora measured from disarticulated skeletal specimens of four anuran taxa (Bufonidae: Anaxyrus americanus, Rhinella marina; Ranidae: Lithobates catesbeianus, Lithobates clamitans). Our findings were consistent with the hypothesis that natural selection for increased locomotor performance may influence patterns of FA seen in vertebrate limbs, with all species displaying lower mean FA in the hindlimbs. More subtle functional roles between the forelimbs of bufonids and ranids, however, did not elicit different levels of FA.     

How to compare fluctuating asymmetry of different traits

Comparing fluctuating asymmetry (FA) between different traits can be difficult because traits vary at different scales. FA is generally quantified either as the variance of the difference between left and right (σ²_L?R) or the mean of the absolute value of this difference (μ_|R?L|). Corrections for scale differences are obtained by dividing by trait size mean. We show that a third index, one minus the correlation coefficient between left and right (1 ? r_L,R), is equivalent to σ²_L?R standardized by trait size variance. The indices are compared with Monte‐Carlo simulations. All achieve the expected correction for scale differences. High type I error rates (false indication of differences) occur only for σ²_L?R and μ_|R?L| if trait sizes close to or below 0 occur. 1 ? r_L,R with a bootstrap test has always low error rates. Recommendation of the index to be used should be based on whether standardization of FA by trait size mean or trait size variance is preferred. A survey of 36 traits in the Speckled Wood Butterfly (Pararge aegeria) indicated that σ²_L?R is slightly higher correlated to trait size variance than to trait size mean. Thus 1 ? r_L,R seems to be the superior index and should be reported when FA of different traits is compared.     

Heat shock in the developmentally sensitive period of butterfly eyespots fails to increase fluctuating asymmetry

Fluctuating asymmetry (FA) is considered to provide a means of evaluating developmental stability and to reflect an individual's quality or the stress experienced during development. Stress is predicted to increase the phenotypic variation of both FA and trait size. In this study we examined the effect of a particular heat shock on both FA and size of eyespots in the butterfly, Bicyclus anynana. We also examined whether those eyespots thought to be involved in partner choice and sexual selection were particularly sensitive to stress. We applied a heat shock of 39.5 degrees C for 3 h before, during, and after a sensitive period in eyespot development. We examined the FA, variation in FA, size, and variation in size of five eyespots, two on the dorsal forewing (sexually selected traits), two on the ventral forewing, and one on the ventral hindwing (nonsexually selected traits). For each sex and treatment, the heat shock did not result in significant changes in mean trait size and FA nor in the variation of size and FA. There were no differences in the response to the heat shock between sexually and nonsexually selected traits. We discuss how the increased production of heat shock proteins, including HSP60, may have stabilized development and how this might explain the results.     

Parasites differentially increase the degree of fluctuating asymmetry in secondary sexual characters

The degree of fluctuating asymmetry has been demonstrated to reflect the ability of individuals to cope with different kinds of environmental stress (Parsons 1990). Parasites and diseases are one kind of environmental stress which most individuals encounter during their lifetime. Parasites have also been suggested to play an important role in sexual selection and the development of ornaments, since the full expression of ornaments may reflect the ability of hosts to cope with the debilitating effects of parasites. Here I report for the first time that a parasite, the haematophagous tropical fowl mite Ornithonyssus bursa (Macronyssidae, Gamasida), directly affects the degree of fluctuating asymmetry in a secondary sexual character of its host, the elongated tail of the swallow Hirundo rustica (Aves: Hirundinidae). I experimentally manipulated the mite load of swallow nests during one season by either increasing or reducing the number of mites, or keeping nests as controls. The degree of fluctuating asymmetry was measured in the subsequent year after the swallows had grown new tail ornaments under the altered parasite regime. The degree of fluctuating asymmetry was larger at increasing levels of parasites for male tail length, but not for the length of the shortest tail feather or wing length or for tail and wing length in females. These results suggest that the degree of fluctuating asymmetry in tail ornaments, but not in other feather traits, reliably reveals the level of parasite infestation. This has important implications for the ability of conspecifics to use the size and the expression of ornaments in assessment of phenotypic quality and thus in sexual selection.     

Covariation of fluctuating asymmetry, herbivory and chemistry during birch leaf expansion

Fluctuating asymmetry (FA) is used to describe developmental instability in bilateral structures. In trees, high FA of leaves has been assumed to indicate the level of environmental or genetic stress, and for herbivores leaves from such trees have been shown to be in some cases (though not invariably) of higher quality compared to trees with symmetrical leaves. We demonstrated that FA of birch leaves correlated positively with growth rate of leaves, and with the amount of leaf biomass consumed by larvae of the geometrid Epirrita autumnata. Since asymmetry per se cannot define leaf quality for a herbivore, we determined the biochemical compounds which covary with the degree of foliage FA, in order to elucidate relationships between leaf FA, chemistry and herbivory. High foliar FA was characteristic of birches with high initial concentrations, and rapid seasonal decline in the concentrations of gallic acid and hydrolysable tannins, and with rapid seasonal changes in the concentrations of flavonoid-glycosides and sugars. In contrast, leaf FA was not related to concentrations of proanthocyanidins, protein-bound amino acids or soluble phenylalanine, the precursor of proanthocyanidins and proteins with aromatic amino acids. The positive correlation between leaf FA and consumption by E. autumnata was presumably related to the previously demonstrated compensatory consumption of E. autumnata to high concentrations of foliar gallotannins. Furthermore, sugars are well-known feeding stimulants. We propose that the variable results in studies correlating leaf FA and herbivory may stem from variable chemical associations of FA in different plants and of species-specific effects of compounds on insects. Received: 15 July 1999 / Accepted: 24 September 1999     

The effect of inbreeding on fluctuating asymmetry in Scabiosa canescens (Dipsacaceae)

Developmental instability and fluctuating asymmetry (FA) describe the inability of organisms to correct for random accidents under development and has become a major but controversial topic in evolutionary biology. Theoretical models predict that the level of FA should increase as a result of inbreeding, but empirical results are ambiguous. Moreover, the relationship between fitness and FA is still debated. In the current study, plants from a population of Scabiosa canescens, a locally rare species in southern Sweden, were raised under uniform growth conditions to examine the effects of one-generation of selfing and outcrossing on FA in flower morphology. The level of flower FA was significantly higher (p = 0.038) for inbred progeny than for offspring derived from outcross pollinations. Given that earlier studies of this species have found no negative relation between heterozygosity and FA, the results support the conclusion that expression of deleterious recessive alleles are responsible for the increase of FA. There was no correlation between FA and estimates of five fitness-related traits when estimated at the individual level. However, a companion study found significant inbreeding depression for all fitness traits, and a negative association between FA and fitness could therefore be asserted at the treatment level (inbred/outbred progeny). Hence, FA seems to be useful to predict inbreeding depression in S. canescens, but specific individuals with high fitness cannot be identified based on their FA levels.     

Agropastoral activities increase fluctuating asymmetry in tadpoles of two neotropical anuran species

Agriculture and pasture activities are the main drivers for habitat reduction, directly affecting amphibian assemblages. In the Cerrado, the progress of agricultural and pasture areas negatively affects aquatic environments and their organisms, once the suppression of marginal vegetation reduces the natural protection against allochtone stressors. One possible way to measure the stress level is the Fluctuating Asymmetry (FA), which is calculated based on the deviations in the development of bilateral morphological traits of the organism. Herein, we evaluated whether environments with a higher degree of agropastoral influence and reduced marginal vegetation can increase FA levels in tadpoles of two common and widely distributed anuran species in the Cerrado (Physalaemus cuvieri and Scinax fuscomarginatus). We sampled and classified water bodies according to the percentage of agropastoral land use and marginal vegetation, and measured four morphological traits of tadpoles to evaluate the degree of FA. We found that in environments with intensive agropastoral land use, tadpoles of P. cuvieri and S. fuscomarginatus had higher FA in nostril‐snout distance (NSD). In environments with reduced marginal vegetation, tadpoles of S. fuscomarginatus had higher FA in eye width (EW), but no effect was detected for tadpoles of P. cuvieri. These morphological traits (i.e. nostrils and eyes) are associated to individual fitness of tadpoles. Thus, these developmental deviations can affect species fitness and population homeostasis over time, contributing to generate stochastic population dynamics and increasing the vulnerability of native species to local extinctions. The use of FA as a tool to measure environmental impact on species with potential to be used as bioindicators can contribute to generate and test hypothesis when integrated with long‐term studies.     

Leaf fluctuating asymmetry of common plantain as an indicator of habitat quality

Abstract

Although developmental instability (DI), measured as fluctuating asymmetry (FA), is expected to be positively related to environmental stress and negatively to habitat quality, the pattern found here was the reverse. Developmental instability of leaf traits (leaf width and vein distances within a leaf) was estimated (using two indices of FA: FA₄ and σ_i ²) and compared between three populations of Plantago major L. (Plantaginaceae) from northern Serbia. Two of the populations are from chronically polluted areas (Karaburma & Zemun), while Crni Lug is from an unpolluted, natural area. Results obtained using both FA indices were the same; higher asymmetry levels in the unpolluted area than in the polluted sites, were found for both traits. Between the two polluted sites, FA values were significantly higher in Karaburma site for vein distances within a leaf. Concerning differences in FA₄ values between samples, in two cases, results are similar to those found for σ_i ² values, for vein distances within leaf. These are the first quantitative data on P. major indicating that (i) plants living in the stressful sites are more symmetrical and (ii) leaf FA for plant species with wide ecological distribution such as P. major should be considered as an ‘index of habitat quality.’     

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.     

空间诱变条件下蜜蜂后代的波动性不对称

利用航天搭载的雄蜂精液对处女王进行人工授精,产卵后大量培育后代蜂王;以SP1、SP2及SP3代蜂王后代工蜂为研究对象,考查波动性不对称(fluctuating asymmetry,FA)在不同代次种群中各对称性状间的表现情况。结果表明:SP1、SP2和SP3代工蜂的前翅长及肘脉a均表现出FA,SP1、SP2代的对照组中均未出现,而SP3代的对照组蜂群则全部表现出FA;与对照蜂群相比,空间诱变后代的前翅长及翅脉a的FA值均较高。此外,讨论FA在蜜蜂种群对生态环境适应性上应用以及利用蜜蜂的FA来监测环境污染的可能性及发展前景。     

Environmental stress and fluctuating asymmetry in the grasshopper Chorthippus parallelus (Acrididae: Gomphocerinae)

We examined the effect of agrochemical pollution/fertilisation of the soil and climatic conditions at high altitudes on fluctuating asymmetry (FA) level in hindfemur and forewing lengths of the grasshopper Chorthippus parallelus (Zetterstedt). All traits and samples exhibited ideal FA. Forewings, which are less functionally significant in this species, generally exhibited greater FA than the more functionally significant femora. Forewing FA was also more affected by stress induced by climatic conditions at high altitudes than femur FA. The high altitude sample was the most asymmetric sample for both traits, followed by the two control samples. The two samples from agrochemically contaminated habitats showed the lowest asymmetry in femora and forewings of C. parallelus. These results suggest that high altitude imposes more stress on this grasshopper species than does agrochemical contamination although the stress response was more dramatic in the less functional trait.     

Variation in fluctuating asymmetry levels across a Robertsonian polymorphic zone of the house mouse

Fluctuating asymmetry (FA) levels were assessed within the Barcelona Robertsonian polymorphic zone of Mus musculus domesticus as a measure of developmental instability (DI). This zone is characterized by populations with a reduced diploid number (2n = 27–39) surrounded by others with standard karyotype (2n = 40). Mice were distributed into four classes according to mean diploid number at each collecting site, and differences in their FA levels were studied. Three different FA indices were calculated on interlandmark distances from two major morphogenetic units of the mandible: the teeth and muscular areas. Three kinds of analysis were performed: trait‐by‐trait, considering the two regions separately and pooling all traits. In univariate analyses few differences were detected between classes. Nevertheless, when characters were pooled, differences in FA values were found between one Robertsonian group and standard mice, and between several Robertsonian classes. Teeth area traits showed higher FA levels in Rb I mice, i.e. those geographically close to the standard populations. However, FA levels decreased in more introgressed Robertsonian groups and showed significant differences with Rb I. Muscular area traits showed lower DI levels in the Robertsonian mice, especially those with an intermediate mean diploid number (Rb II). When all traits were pooled, FA levels increased in Rb I, whilst the other Robertsonian groups showed similar, or even lower, FA values to those of the standard mice. The higher FA levels found in Rb I suggest an increase in the disruption of genetic coadaptation. Furthermore, in Rb I the presence of metacentrics is more recent than in more introgressed populations; we therefore suggest that Rb I have had less time to restore genetic coadaptation. In addition, the teeth region of the mandible seems to be more sensitive to genomic stress than the muscular region. In the light of these results we suggest that hybrids should be separated into groups and that mandible morphogenetic units be differentiated when using FA in hybrid zones to analyse DI.     

No relationship between fluctuating asymmetry and fitness in Lychnis viscaria

Several earlier studies have indicated a negative relationship between fluctuating asymmetry (FA) and fitness. We tested this assumption by investigating the association between petal asymmetry and several fitness-related characters among natural and common garden populations of Lychnis viscaria. Neither seed set, germination percentage nor the growth rate of seedlings were related to the level of flower asymmetry either among natural populations or in common garden conditions. The only significant association found was a positive connection between petal asymmetry and seed mass measured from natural populations. Thus, in contrary to many earlier published reports, we did not find any evidence for a negative relationship between FA and fitness even if we controlled for measurement error, we had adequate sample size and we measured these characters in two environments. This suggests that FA is not consistently related to individual quality and fitness.     

Natural genetic variation in fluctuating asymmetry of wing shape in Drosophila melanogaster

Fluctuating asymmetry (FA), defined as random deviation from perfect symmetry, has been used to assay the inability of individuals to buffer their developmental processes from environmental perturbations (i.e., developmental instability). In this study, we aimed to characterize the natural genetic variation in FA of wing shape in Drosophila melanogaster, collected from across the Japanese archipelago. We quantified wing shapes at whole wing and partial wing component levels and evaluated their mean and FA. We also estimated the heritability of the mean and FA of these traits. We found significant natural genetic variation in all the mean wing traits and in FA of one of the partial wing components. Heritability estimates for mean wing shapes were significant in two and four out of five wing traits in males and females, respectively. On the contrary, heritability estimates for FA were low and not significant. This is a novel study of natural genetic variation in FA of wing shape. Our findings suggest that partial wing components behave as distinct units of selection for FA, and local adaptation of the mechanisms to stabilize developmental processes occur in nature.     

Nectar guide fluctuating asymmetry does not relate to female fitness in Mimulus luteus

Most studies assessing the importance of developmental instability of floral characters for pollinator visits and plant fitness have focused on the fluctuating asymmetry (FA) of the corolla phenotype. The importance of stability process for nectar guide characters that signal floral reward has not been considered in the literature. In principle, flowers with symmetrical guides should be more successful at attracting pollinators, therefore increasing their reproductive success in comparison to asymmetrical flowers. In this paper we test this hypothesis in a population of 171 individuals of the Andean monkey flower, Mimulus luteus in northern Chile. This species shows a conspicuous red spot in the landing yellow petal, which permits assessment of the functional relationship between nectar guide FA and female fitness. Our results did not reveal a significant linear nor nonlinear relationship between nectar guide FA and fitness. This result was consistent after controlling the level of FA by guide and corolla size. Because the corolla of M. luteus did not show evidence of UV wavelength reflectance, our negative result could not be attributable to a confounding effect of UV guides. Even though we can not rule out that nectar guide FA correlates better with male than female fitness, the low fraction of the variance in female fitness accounted for nectar guide FA, suggests that other components of the floral phenotype as well as environmental factors may be more important to predict pollinator preference and reproductive success in this species. This revised version was published online in June 2006 with corrections to the Cover Date.     

Environmental stress increases skeletal fluctuating asymmetry in the moor frog Rana arvalis

Whether fluctuating asymmetry (FA) provides a useful metric indicator of the degree of environmental stress experienced by populations is still a contentious issue. We investigated whether the degree of FA in skeletal elements is useful in elucidating the degree of environmental stress experienced by frog populations, and further, tested the proposition that a trait’s sensitivity to stress—as reflected in the degree of FA—is related to the degree of directional selection experienced by the given trait. We compared the degree of FA in four bilateral skeletal elements of male and female moor frogs (Rana arvalis) originating from low (acidified) and neutral pH populations. While the degree of uncorrected FA was unrelated to the degree of acidity, the growth rate and age of the individuals, the size-corrected FA was significantly higher in low than in neutral pH populations and decreased with individual ages and growth rates. In addition, both measures of FA were significantly higher in males and in particular in traits presumably under high sexual selection as indicated by the degree of sexual size dimorphism. All in all, the results indicate that individuals from acidified localities are smaller, younger and exhibit a significantly higher degree of FA than individuals from neutral pH populations. These results constitute the first assessment of FA in amphibians and suggest that the degree of FA in skeletal traits can be a useful indicator of the degree of environmental stress experienced by amphibian populations.