Fluctuating asymmetry in the otoliths of larval fish as an indicator of condition: conceptual and methodological aspects

Developmental instability, measured as fluctuating asymmetry (FA) in bilateral traits, has been used widely as an indicator of genetic or environmental stress in a variety of plant and animal taxa. FA arises as small deviations from perfect bilateral symmetry which reflect 'mistakes' in developmental processes resulting from the inability of the genotype to buffer itself effectively against environmental perturbations. Recently, it has been proposed that FA in the otoliths can be used as an indicator of condition in larval fish. This paper reviews the conceptual and methodological aspects of FA relevant to its potential use as a measure of well-being. Its simplicity makes FA an attractive tool to measure developmental precision and condition. However, there are several pitfalls, such as measuring error or potentially size dependence. Subtle asymmetries, i.e. between sides variation of a trait at the individual level, may not always be indicative of condition and should be interpreted with caution. The past-growth record of otoliths may provide a powerful means of studying the development of asymmetries at the level of the individual.     

Fluctuating asymmetry,body size and sexual selection in the dung fly Sepsis cynipsea — testing the good genes assumptions and predictions

In the dung fly Sepsis cynipsea large and more symmetric males have been shown to enjoy a mating advantage, but we still do not know which mechanism of sexual selection is responsible. Here we test several assumptions and predictions relating to the hypothesis that either trait is indicative of ‘good genes’. We tested for good genes by regressing fitness in good and bad environments (no and high larval competition, respectively) on the family mean for size or asymmetry as expressed in the good environment, separately for both sexes. Body size (hind tibia length or head width) was positively correlated with female fecundity, growth rate of both sexes and larval survivorship for males, but only in the good environment. The corresponding evidence for asymmetry is more equivocal. Mean standardised asymmetry was weakly associated with lower survivorship in the good environment, while growth rates and female fecundity were not. As predicted by sexual selection theory, fore tibia length showed greater asymmetry than other, presumably not sexually selected traits, and asymmetry in fore tibia length was greater for males than females. However, a negative correlation between trait size and asymmetry was only evident for male seta length but not for fore tibia length, fore femur length, or any composite measure of asymmetry. Most crucially, asymmetry was heritable for some female morphological traits (hind tibia length: h² = 0.15; fore femur length: h² = 0.16; mean of all measured traits: h² = 0.27), but not for any male trait. Also, asymmetry of the various traits measured was not correlated within males and only weakly so within females. The crucial assumption that asymmetry of sexually selected traits reflects overall, heritable developmental stability of an individual is thus only partly substantiated by our data. In contrast, large body size is heritable, associated with high fitness and consequently could be indicative of good genes. Fore leg asymmetry may influence male mating success by simply mechanically constraining his ability to hold on to the female.     

Fluctuating asymmetry in a secondary sexual trait: no associations with individual fitness, environmental stress or inbreeding, and no heritability

It has been suggested that fluctuating asymmetry (FA) in secondary sexual traits may be a useful indicator of either individual quality or environmental stress. We tested this concept using a series of analyses of FA in male antler size in a wild red deer (Cervus elaphus) population, using four measures of size repeated across successive years on the same individuals. We found no consistent evidence of correlations between traits in levels of FA, nor of any associations between known environmental or developmental conditions. None of the four measures of FA showed a significant heritability (average h2 = 0.041), nor was there any evidence of inbreeding depression. For three of the four traits, fluctuating asymmetry did not predict either annual or lifetime breeding success. However there were significant associations between breeding success and FA in antler length. Given the series of null results in our other tests, it seems likely that this was a direct mechanistic effect rather than because measures of FA were indicative of individual quality or condition.     

Individual differences in developmental precision and fluctuating asymmetry: a model and its implications

In many studies, fluctuating asymmetry (FA) has been used as a measure of individual differences in developmental imprecision. A model of how variation in developmental imprecision is associated with variation in asymmetry is described and applied to important issues about FA. If individual differences in developmental imprecision exist, asymmetry due to developmental error should be leptokurtically distributed. Moreover, the greater the magnitude of individual differences, the greater the leptokurtosis. Asymmetry purportedly due to developmental error in a variety of species is indeed leptokurtically distributed. The level of leptokurtosis suggests that the CV in individual differences in underlying developmental imprecision is generally 20–25, consistent with it being a fitness trait. In addition, data suggest that: (1) the individual differences that underlie the developmental imprecision of different traits are largely shared across traits and not trait-specific; (2) the heritability of these individual differences may average between 35 and 55%, despite small heritabilities of individual trait FAs; and (3) correlations between FA and fitness traits or components suggest high correlations between underlying variation in developmental precision and fitness in many species. Theoretical implications are discussed.     

Maternal body condition influences magnitude of anti-predator response in offspring

Organisms exhibit plasticity in response to their environment, but there is large variation even within populations in the expression and magnitude of response. Maternal influence alters offspring survival through size advantages in growth and development. However, the relationship between maternal influence and variation in plasticity in response to predation risk is unknown. We hypothesized that variation in the magnitude of plastic responses between families is at least partly due to maternal provisioning and examined the relationship between maternal condition, egg provisioning and magnitude of plastic response to perceived predation risk (by dragonfly larvae: Aeshna spp.) in northern leopard frogs (Lithobates pipiens). Females in better body condition tended to lay more (clutch size) larger (egg diameter) eggs. Tadpoles responded to predation risk by increasing relative tail depth (morphology) and decreasing activity (behaviour). We found a positive relationship between morphological effect size and maternal condition, but no relationship between behavioural effect size and maternal condition. These novel findings suggest that limitations imposed by maternal condition can constrain phenotypic variation, ultimately influencing the capacity of populations to respond to environmental change.     

Maternal nutritional condition and genetic differentiation affect brood size and offspring body size in Nicrophorus

In most animal species, brood size and body size exhibit some variation within and between populations. This is also true for burying beetles (genus Nicrophorus), a group in which the body size of offspring depends critically on the number of offspring competing for food due to the discrete nature of resource used for larval nutrition (vertebrate carcasses). In one species, brood size and body size are correlated with population density, and appear to be phenotypically plastic. We investigated potential proximate causes of between-population variation in brood size and body size in two species, Nicrophorus vespilloides and Nicrophorus defodiens. Our first experiment supported the notion that brood size is phenotypically plastic, because it was affected by environmental variation in adult nutritional condition. We found that the pre-breeding nutritional status of female N. vespilloides affected the number of eggs they laid, the number of surviving larvae in their broods, and the body size of their offspring. We do not know whether this plasticity is adaptive because greater offspring body size confers an advantage in contests over breeding resources, or whether starved females are constrained to produce smaller clutches because they cannot fully compensate for their poor pre-breeding nutritional status by feeding from the carcass. Our second experiment documents that brood size, specifically the infanticidal brood-size adjustment behavior, has undergone genetic differentiation between two populations of N. defodiens. Even under identical breeding conditions with identical numbers of first-instar larvae, females descended from the two populations produced broods of different size with corresponding differences in offspring body size.     

Relationships between tail-flicking, morphology, and body condition in Moorhens

ABSTRACT.   Prey-predator communication of alertness has been reported for Moorhens ( Gallinula chloropus ) and other species of birds. Because ability to flee is probably related to body condition, healthy potential prey may behave more conspicuously to send predators an unambiguous message. Moorhens have a contrasting rump patch that is flashed by rapid tail-flicking. During two winter months, we observed sex-related differences in the rate of tail-flicking. Females tail-flicked at a faster rate than males, and more vigilant and more symmetrical males tail-flicked faster. The rate of tail-flicking was negatively correlated to the heterophil/lymphocyte ratio in both sexes and positively correlated to hematocrit and albumin/globulin ratio in females. These results suggest that male and female Moorhens in better physical condition tail-flick at a faster rate and support the pursuit deterrent hypothesis, with healthy individuals appearing to inform predators that they would be difficult to capture.     

A simple model of the relationship between asymmetry and developmental stability

The relationship between developmental stability and morphological asymmetry is derived under the standard view that structures on each side of an individual develop independently and are normally distributed. I use developmental variance of sizes of parts, V_D, as the converse of developmental stability, and assume that V_D follows a gamma distribution. Repeatability of asymmetry, a measure of how informative asymmetry is about V_D, is quite insensitive to the variance in V_D, for example only reaching 20% when the coefficient of variation of V_D is 100%. The coefficient of variation of asymmetry, CV_FA, also increases very slowly with increasing population variation in V_D. CV_FA values from empirical data are sometimes over 100%, implying that developmental stability is sometimes more variable than any previously studied type of trait. This result suggests that alternatives to this model may be needed.     

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。     

Fluctuating asymmetry of sexual and nonsexual traits in stalk‐eyed flies: a poor indicator of developmental stress and genetic quality

It has been proposed that females use fluctuating asymmetry (FA) in sexual ornaments to assess male quality. FA of sexual traits is predicted to show greater sensitivity to stress than FA of nonsexual traits, and to be heritable. We used a half‐sib mating design and manipulation of larval food environment to test these predictions on stalk‐eyed flies, Cyrtodiopsis dalmanni, in which females prefer males with larger eyespans. We measured size and FA of eyestalks and of two nonsexually selected characters, wing length and width. We found no evidence of an increase in FA under larval food stress in any of the individual traits, although trait size decreased under stress. We combined FA across traits into a single composite index, and found that males reared in the most benign larval environment had significantly higher composite FA than males reared on other media. There was no such effect in females. Heritability of FA was not significantly different from zero in any of the traits, in any of the environments, although trait sizes showed high heritability. We conclude that FA in sexual and nonsexual traits is a poor indicator of developmental stress and genetic quality.     

SIZE,SYMMETRY, AND SEXUAL SELECTION IN THE HOUSEFLY,MUSCA DOMESTICA

Relationships between measures of body size, asymmetry, courtship effort, and mating success were investigated in the housefly, Musca domestica (Diptera: Muscidae). A previous study indicated that both male and female flies with low fluctuating asymmetry enjoyed enhanced mating success. The aim of our investigations was to determine whether the greater success of symmetrical males is due to variation in male mating effort or to female choice and whether males exhibited mate choice. However, our study found directional rather than fluctuating asymmetry with both male and female flies having, on average, longer left wings than right. Also, asymmetry was not related to mating success in either sex. Rather, both males and females appeared to exhibit choice on the basis of the size of potential mates, with males preferring females with long bodies and females preferring heavy males. Possible benefits from choice of large mates are discussed. The initial mating strikes (in which the male leaps onto the back of the female) did not appear to be targeted according to female morphology, and their frequency did not vary according to male morphology. This indicates that mate choice by both sexes according to size probably occurs during the later stages of courtship, when the flies are in intimate contact. Possible reasons for the absence of choice according to asymmetry are discussed.     

Impact of a population bottleneck on symmetry and genetic diversity in the northern elephant seal

Abstract The northern elephant seal (NES) suffered a severe population bottleneck towards the end of the nineteenth century. Theoretical expectations for the impact of population bottlenecks include the loss of genetic diversity and a loss of fitness (e.g. through a disruption of developmental stability); however, there are few direct demonstrations in natural populations. Here, we report on the comparison of archive samples collected prior to and following the NES population bottleneck. Measures of genetic diversity show a loss of variation consistent with expectations and suggest a strong disruption in the pattern of allele frequencies following the bottleneck. Measures of bilateral characters show an increase in fluctuating asymmetry.     

Estimation of Developmental Stability of Small-Leaved Lime on Reserved and Urbanized Territories

The developmental stability of small-leaved lime (Tina cordata Mill.) was estimated in populations on territories of the Kerzhenskii State Nature Reserve, Nizhni Novgorod District, and in an industrial region of Nizhni Novgorod. The developmental stability was estimated according to the fluctuating asymmetry of the leaf measurements. The results obtained suggest that, in the urbanized territory, the homeostatic developmental mechanisms are weakened, as expressed in the increased degree of leaf asymmetry.     

Comparing developmental stability in unisexual and bisexual rock lizards of the genus Darevskia

Parthenogenetic species are usually considered to be short‐lived due to the accumulation of adverse mutations, lack of genetic variability, and inability to adapt to changing environment. If so, one may expect that the phenotype of clonal organisms may reflect such genetic and/or environmental stress. To test this hypothesis, we compared the developmental stability of bisexual and parthenogenetic lizards of the genus Darevskia. We assessed asymmetries in three meristic traits: ventral, preanal, and supratemporal scales. Our results suggest that the amount of ventral and preanal asymmetries is significantly higher in clones compared with their maternal, but not paternal, progenitor species. However, it is questionable, whether this is a consequence of clonality, as it may be considered a mild form of outbreeding depression as well. Moreover, most ventral asymmetries were found in the bisexual species Darevskia valentini. We suggest that greater differences in asymmetry levels among bisexuals may be, for instance, a consequence of the population size: the smaller the population, the higher the inbreeding and the developmental instability. On the basis of the traits examined in this study, the parthenogens do not seem to be of significantly poorer quality.     

Variational and genetic properties of developmental stability in Dalechampia scandens

Because low developmental stability may compromise the precision with which adaptations can be reached, the variability and genetic basis of developmental stability are important evolutionary parameters. Developmental stability is also an important clue to understanding how traits are regulated to achieve their phenotypic target value. However, developmental stability must be studied indirectly through proxy variables, such as fluctuating asymmetry, that are suggested to have noisy and often nonlinear relationships to the underlying variable of interest. In this paper we first show that mean-standardized measures of variance and covariance in fluctuating asymmetry, unlike heritabilities, repeatabilities, and correlations, are linearly related to corresponding measures of variation in underlying developmental stability. We then examine the variational properties of developmental stability in a population of the Neotropical vine, Dalechampia scandens (Euphorbiaceae). By studying fluctuating asymmetry in a large number of floral characters in both selfed and outcrossed individuals in a diallel design, we assemble strong evidence that both additive genetic and individual variation and covariation in developmental stability are virtually absent in this population.     

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

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

Modelling developmental instability in relation to individual fitness: a fully Bayesian latent variable model approach

Since the influential paper by Palmer and Strobeck in 1986, the statistical analysis of fluctuating asymmetry and developmental stability has received much attention. Most studies deal with one of the following four difficulties: (i) correcting for bias in asymmetry estimates due to measurement error; (ii) quantifying sampling error in the estimation of individual developmental stability using individual asymmetry; (iii) the detection of directional asymmetry and antisymmetry; and (iv) combining data from several traits. Yet, few studies have focused on statistical properties of estimating a relationship between individual developmental stability and other factors (e.g. fitness). In this paper I introduce a fully Bayesian model in which the unobservable individual developmental stability is treated as a latent variable. The latter is then related to individual fitness. I show by means of the analysis of simulated data that this approach has several advantages over traditional techniques. First, the method provides unbiased (but slightly less accurate) estimates of slopes between developmental stability and fitness taking all sources of error into account. Secondly, it allows proper investigation of non‐linear associations. Finally, the model allows unbiased estimation of unobserved fitness of individuals that have been measured on left and right side.     

Variation patterns of bilateral characters: variation among characters and among populations in the White Sea herring, Clupea pallasi marisalbi (Berg) (Clupeidae, Teleosti)

Phenotypic variation in two populations of the White Sea herring Clupea pallasi marisalbi (Berg) (spring spawners and summer spawners), based on 21 meristic and 21 morphometric bilateral characters, has been studied. Total phenotypic variance was partitioned into a within-individual or stochastic component (fluctuating asymmetry) and an among-individual or factorial component, reflecting heterogeneity among individuals and resulting from the diversity of genotypes and environments. Both standardized stochastic and factorial components show clear negative correlations with means across characters. Negative correlation of the factorial components with means is in contradiction to the commonly accepted explanation of negative means-standardized variances association. Slopes of regression of standardized stochastic variances on means in meristic characters was significantly higher in summer spawners than in spring spawners, and results in discordance of stochastic variance across characters: it is higher in spring spawners for low and average variability characters and does not differ for both populations for high variability characters. The populations do not show notable differences in variation of morphometric characters. Consideration of other available data on these populations, such as spawning behaviour and salinity resistance of larvae, suggests that the lower slope of regression of stochastic variances on means is associated with the reduced viability of spring spawners