Measuring fitness and intergenic interactions: The evolution of resistance to diazinon inLucilia cuprina

Resistance at the diazinon-resistance locus (Rop-1) is recessive with respect to fitness. Selection initially occurs at concentrations lower than those required to controlLucilia cuprina. The presence of theRop-1 allele initially disrupted development so that in the absence of diazinon, carriers were at a relative selective disadvantage. Continued use of the chemical, subsequent to resistance evolving, selected a modifier to ameliorate this effect. Modified resistant phenotypes show similar developmental stability and relative fitness to susceptible individuals. Frequency-dependent interactions are observed between resistant and susceptible phenotypes of theRop-1 locus. The interactions are determined by the concentration of diazinon and range from competitive to facilitative. The results are discussed in the context of the contribution insecticide resistance systems can make to the study of general evolutionary phenomena.     

Diazinon resistance, fluctuating asymmetry and fitness in the Australian sheep blowfly, lucilia cuprina

Genetic evidence suggests that the evolution of resistance to the insecticide diazinon in Lucilia cuprina initially produced an increase in asymmetry. At that time resistant flies were presumed to be at a selective disadvantage in the absence of diazinon. Subsequent evolution in natural populations selected modifiers to ameliorate these effects. The fitness and fluctuating asymmetry levels of resistant flies are currently similar to those of susceptibles. Previous genetic analyses have shown the fitness modifier to co-segregate with the region of chromosome III marked by the white eyes, w, locus, unlinked to the diazinon resistance locus, Rop-1, on chromosome IV. This study maps the asymmetry modifier to the same region, shows, as in the case of the fitness modifier, its effect to be dominant and presents data consistent with the fitness/asymmetry modifier being the same gene (gene complex). These results suggest changes in fluctuating asymmetry reflect changes in fitness.     

Environmental and Genetic Effects on the Asymmetry Phenotype: Diazinon Resistance in the Australian Sheep Blowfly, Lucilia Cuprina

The asymmetry phenotype of diazinon-resistant flies lacking a fitness/asymmetry Modifier (+/+; R/-) was dominant and independent of developmental temperature, larval density and diazinon concentration. Asymmetry score, pooled over three bristle characters, was ~50% greater for these phenotypes than for those of modified genotypes (M/-; -/-) and unmodified susceptibles (+/+; S/S) reared under standard laboratory conditions. Modified and susceptible phenotypes showed increased asymmetry score for temperatures and larval densities above and below standard rearing conditions; a positive correlation was observed between diazinon concentration and asymmetry score. Single and multiple environmental stresses resulted in similar scores that approached, but never exceeded, those of unmodified resistant phenotypes. Irrespective of the developmental conditions anti-symmetry and fluctuating asymmetry were typically observed for each bristle character of unmodified resistant and the modified and susceptible phenotypes, respectively. Thus while similar asymmetry scores could arise from genetic or environmental effects, asymmetry pattern was genetically based. Population cage analyses at different temperatures and larval densities showed a negative association between mean asymmetry and relative fitness.     

Herbivore effects on developmental instability and fecundity of holm oaks

Plants are able to compensate for loss of tissue due to herbivores at a variety of spatial and temporal scales, masking detrimental effects of herbivory on plant fitness at these scales. The stressing effect of herbivory could also produce instability in the development of plant modules, and measures of such instability may reflect the fitness consequences of herbivory if instability is related to components of plant fitness. We analyse the relationships between herbivory, developmental instability and production of female flowers and fruits of holm oak Quercus ilex trees by means of herbivore removal experiments. Removal of leaf herbivores reduced herbivory rates at the tree level, but had no effect on mean production of female flowers or mature fruits, whereas herbivory tended to enhance flower production and had no effect on fruit abortion at the shoot level. Differences in herbivory levels between shoots of the same branch did not affect the size and fluctuating asymmetry of intact leaves. These results indicate compensation for herbivory at the tree level and over-compensation at the shoot level in terms of allocation of resources to female flower production. Removal of insect herbivores produced an increase in the mean developmental instability of leaves at the tree level in the year following the insecticide treatment, and there was a direct relationship between herbivory rates in the current year and leaf fluctuating asymmetry the following year irrespective of herbivore removal treatment. Finally, the production of pistillate flowers and fruits by trees was inversely related to the mean fluctuating asymmetry of leaves growing the same year. Leaf fluctuating asymmetry was thus an estimator of the stressing effects of herbivory on adult trees, an effect that was delayed to the following year. As leaf fluctuating asymmetry was also related to tree fecundity, asymmetry levels provided a sensitive measure of plant performance under conditions of compensatory responses to herbivory.     

Trisomy 21 and facial developmental instability

The most common live‐born human aneuploidy is trisomy 21, which causes Down syndrome (DS). Dosage imbalance of genes on chromosome 21 (Hsa21) affects complex gene‐regulatory interactions and alters development to produce a wide range of phenotypes, including characteristic facial dysmorphology. Little is known about how trisomy 21 alters craniofacial morphogenesis to create this characteristic appearance. Proponents of the "amplified developmental instability" hypothesis argue that trisomy 21 causes a generalized genetic imbalance that disrupts evolutionarily conserved developmental pathways by decreasing developmental homeostasis and precision throughout development. Based on this model, we test the hypothesis that DS faces exhibit increased developmental instability relative to euploid individuals. Developmental instability was assessed by a statistical analysis of fluctuating asymmetry. We compared the magnitude and patterns of fluctuating asymmetry among siblings using three‐dimensional coordinate locations of 20 anatomic landmarks collected from facial surface reconstructions in four age‐matched samples ranging from 4 to 12 years: 1) DS individuals (n = 55); 2) biological siblings of DS individuals (n = 55); 3) and 4) two samples of typically developing individuals (n = 55 for each sample), who are euploid siblings and age‐matched to the DS individuals and their euploid siblings (samples 1 and 2). Identification in the DS sample of facial prominences exhibiting increased fluctuating asymmetry during facial morphogenesis provides evidence for increased developmental instability in DS faces. We found the highest developmental instability in facial structures derived from the mandibular prominence and lowest in facial regions derived from the frontal prominence. Am J Phys Anthropol 151:49–57, 2013. © 2013 Wiley Periodicals, Inc.     

ANALYSIS OF GENOTYPIC DIFFERENCES IN DEVELOPMENTAL STABILITY IN ANNONA CHERIMOLA

The genetic basis of developmental stability, measured as asymmetry (fluctuating asymmetry in leaves), was analyzed in leaves and flowers of cherimoya (Annona cherimola Mill) and atemoya (A. cherimola × A. squamosa). The individuals analyzed belonged to a controlled collection of cultivars (clones) that had previously been characterized by means of isozymes. We used a nested design to analyze the differences in asymmetry at several sampling levels: individual leaves and flowers, individual trees, and genotypes. The clonal repeatability of developmental stability was not significantly different from zero, thus suggesting the absence of heritability of the asymmetry for leaves and flowers under these environmental conditions. No relationship between asymmetry and individual heterozygosity was found, but leaf fluctuating asymmetry was significantly related to particular isozymic genes. Petal and leaf size showed a phenotypically plastic response to the exposure zone of the tree (mainly due to light). Leaf fluctuating asymmetry also showed such a plastic response. No significant correlation was found between asymmetry and any pomological characters (some of these being fitness related). Finally, the hybrid species (atemoya) did not show larger developmental instability than did the parental species (cherimoya). All these data show that cherimoya asymmetry reveals the random nature of developmental noise, with developmental stability for leaves being possibly related to specific chromosome regions, but with weak evidence for genotypic differences in developmental stability.     

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.     

Zinc and cadmium accumulation in cabbage aphid (Brevicoryne brassicae) host plants and developmental instability

Developmental instability in morphological characters can occur during individual development due to various environmental stresses. Fluctuating asymmetry (FA) is often used as a measurement of developmental instability, but within-environment variation (CV_e) is also considered an indicator of developmental instability. Cabbage aphid ( Brevicoryne brassicae ) populations were reared on zinc- (Zn) or cadmium- (Cd) contaminated cabbage and radish plants. Developmental instability indicators were measured and their relations with fitness were explored. Results revealed that cabbage aphids exposed to Cd and Zn displayed considerable developmental instability, particularly fluctuating asymmetry. Differences in developmental instability between the two metals were also detected, as well as differences between the two developmental instability measurements. For almost all measured traits, FA was greater on Cd- and Zn-contaminated compared to non-contaminated host plants. In contrast, CV_e of some traits was greater on non-contaminated host plants, yet for other traits CV_e was greater on contaminated host plants. There were also non-significant inverse relationships between FA and fitness of cabbage aphid populations. Due to weak correlations between FA and different patterns of two developmental instability measurements, this study does not support the hypothesis that developmental instability is a useful bioindicator of environmental quality.     

Fluctuating and directional asymmetry in natural bird populations exposed to different levels of habitat disturbance, as revealed by mixture analysis

While bilateral trait asymmetry is widely recognized to estimate developmental instability, much controversy exists over which types of asymmetry (fluctuating, directional, and/or antisymmetry) to use. Recently it has been hypothesized that the three types are strongly interrelated, and that increased developmental instability may be reflected in a transition from fluctuating to directional asymmetry and/or antisymmetry. Alternatively, habitat disturbance might change the genetic expression of directional asymmetry. We present herein the first empirical evidence for stress-mediated shifts in types of asymmetry in natural populations, by using mixture analysis to model tarsus asymmetry in bird populations exposed to different levels of habitat disturbance. Observed asymmetry patterns almost exclusively consisted of true fluctuating asymmetry in the least disturbed populations, but became progressively mixed with directional asymmetry under increasing disturbance. Failing to unravel these mixtures of different forms of asymmetry may have critical implications for the analysis and interpretation of asymmetry data.     

Fluctuating asymmetry and fitness in Drosophila melanogaster

Models predict that developmental stability measured by fluctuating asymmetry should be positively correlated with fitness. Although such a correlation has often been suggested by indirect studies, there is still a lack of direct experimental evidence. In this note, I have measured the fluctuating asymmetry of sternopleural bristle counts in 32 lines of Drosophila melanogaster sharing the same genetic background but displaying all combinations of five visible mutations. Fluctuating asymmetry was heterogeneous among lines, suggesting a direct impact of the mutations on developmental stability. Two measures of fitness were made for each line: productivity (a combined measure of fecundity and egg‐to‐adult survivorship) and competitive male mating success. Fluctuating asymmetry was correlated with neither of these two components of fitness. This suggests that generalizations about fluctuating asymmetry must be taken with care.     

DEVELOPMENTAL STABILITY OF RAINBOW TROUT HYBRIDS: GENOMIC COADAPTATION OR HETEROZYGOSITY?

I compare the developmental stability of first generation hybrids between hatchery strains of rainbow trout (Salmo gairdneri) to that of the three pure parental strains raised in a common environment. Two of three reciprocal hybrid pairs show significantly less fluctuating asymmetry of four meristic characters than is found in parental strains. In contrast, the third hybrid pair shows reduced but not significantly lower developmental stability compared to pure strains. These hybrids had previously been found to develop slower than their maternal parental strains, indicating divergence of parental regulatory mechanisms controlling early ontogeny. A significant positive association between the degree of relative delay in hybrid developmental rate and their degree of developmental instability supports this view. For example, the only hybrid pair with decreased developmental stability also had the largest relative delay in development time of all hybrids. Neither absolute developmental rate nor enzyme heterozygosity at 42 loci alone can explain the degree of fluctuating asymmetry in these hybrids. The developmental stability of hybrids is apparently a result of the interaction between the developmental divergence between parental strains and their genomic heterozygosity due to hybridization.     

Asymmetry patterns across the distribution range: does the species matter?

An important question in evolutionary ecology is whether different populations across a species range, from core to periphery, experience different levels of stress. The estimation of developmental instability has been proposed as a useful tool for quantifying the degree of environmental and genetic stress that individuals experience during their development. Fluctuating asymmetry, the unsigned difference between the two sides of a bilaterally symmetrical trait, has been suggested to reflect the levels of developmental instability in a population. As such, it has been proposed as a useful tool for estimating changes in developmental instability and in stress response in populations across a range of environmental conditions. Recent studies focusing mostly on birds have detected increasing fluctuating asymmetry from core to periphery across the distribution range, suggesting that peripheral populations may experience higher levels of environmental and/or genetic stress. Most of these comparisons were done for single taxa across a single gradient. However, different species are predicted to respond differently to environmental shifts across the range. We compared asymmetry patterns in wing morphology in populations of two Euchloe butterfly species across their opposing ranges in Israel. Contrary to the patterns observed in birds across the same gradient, bilateral asymmetry did not increase or shift towards the periphery in either of the butterfly species. If fluctuating asymmetry in these traits reflects levels of stress, these results may partly reflect the fact that the range of these two butterfly species is limited by the distribution of their host plant, rather than by abiotic environmental variables. In addition, developing pierids can diapause during harsh seasons and can persist in resource‐rich patches, thus minimizing the environmental stress perceived by developing individuals. We conclude that accounting for differences in species’ life histories and range‐limiting factors is necessary in order to better predict patterns of developmental instability across spatial and environmental gradients. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 81 , 313–324.     

Asymmetric size and shape variation in the Central European transect across the house mouse hybrid zone

We studied asymmetric variation of the mandible in the Central European portion of the hybrid zone between two house mouse subspecies, Mus musculus musculus and Mus musculus domesticus. Within introgression classes, defined by the share of diagnostic allozymes, we quantified the directional and fluctuating component of asymmetric variation, as well as skewness and kurtosis of individual asymmetry distributions. Furthermore, in the same manner we re‐analysed asymmetric variation of the ventral side of the skull. According to the quadratic polynomial model, the mandible shape‐fluctuating asymmetry, but not size‐fluctuating asymmetry, was significantly decreased in the centre of the hybrid zone (with a minimum predicted for a hybrid index of 0.41). On the contrary, the skull shape‐fluctuating asymmetry non‐monotonically increased towards the musculus side of the hybrid zone (with a peak predicted for a hybrid index of 0.86). Thus, the impact of hybridization on fluctuating asymmetry is trait‐specific in this portion of the house mouse hybrid zone. The only general feature of asymmetric variation we observed was the shift towards the platykurtosis of asymmetry distributions in the centre of the hybrid zone. Taken together, we suggest genetic variability for right–left asymmetries to be generally increased, but the developmental instability of mandible shape to be decreased, by hybridization. We hypothesize the decrease of developmental instability to be caused by overdominant effects on developmental dynamics rather than by increased heterozygosity. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 13–27.     

Developmental stability and fitness: a review

Developmental stability reflects the ability of individuals to undergo stable development of their phenotype under a range of environmental conditions. Developmental instability is measured in terms of fluctuating asymmetry or phenodeviance. A negative relationship between developmental instability and fitness has figured as a prominent untested assumption in the literature. A review of available information from the literature on the relationship between developmental instability and various fitness components such as growth, fecundity, and longevity suggests that there indeed is a general negative relationship. Symmetrical individuals do generally have faster growth, higher fecundity, and better survival than do more asymmetrical individuals. These differences appear partially to arise from lower competitive ability and higher risks of predation and parasitism of asymmetrical individuals compared with more symmetrical conspecifics. The relationship between developmental stability and fitness may be either direct or indirect.     

Fluctuating asymmetry as an indicator of fitness: can we bridge the gap between studies?

There is growing evidence from both experimental and non-experimental studies that fluctuating asymmetry does not consistently index stress or fitness. The widely held--yet poorly substantiated--belief that fluctuating asymmetry can act as a universal measure of developmental stability and predictor of stress-mediated changes in fitness, therefore staggers. Yet attempts to understand why the reported relationships between fluctuating asymmetry, stress and fitness are so heterogeneous--i.e. whether the associations are truly weak or non-existent or whether they become confounded during different stages of the analytical pathways remain surprisingly scarce. Hence, we attempt to disentangle these causes, by reviewing the various statistical and conceptual factors that are suspected to confound potential relationships between fluctuating asymmetry, stress and fitness. Two main categories of factors are discerned: those associated with the estimation of developmental stability through fluctuating asymmetry and those associated with the effects of genotype and environment on developmental stability. Next, we describe a series of statistical tools that have recently been developed to help reduce this noise. We argue that the current lack of a theoretical framework that predicts if and when relationships with developmental stability can be expected, urges for further theoretical and empirical research, such as on the genetic architecture of developmental stability in stressed populations. If the underlying developmental mechanisms are better understood, statistical patterns of asymmetry variation may become a biologically meaningful tool.     

GEOMETRIC MORPHOMETRICS OF DEVELOPMENTAL INSTABILITY: ANALYZING PATTERNS OF FLUCTUATING ASYMMETRY WITH PROCRUSTES METHODS

Although fluctuating asymmetry has become popular as a measure of developmental instability, few studies have examined its developmental basis. We propose an approach to investigate the role of development for morphological asymmetry by means of morphometric methods. Our approach combines geometric morphometrics with the two-way ANOVA customary for conventional analyses of fluctuating asymmetry and can discover localized features of shape variation by examining the patterns of covariance among landmarks. This approach extends the notion of form used in studies of fluctuating asymmetry from collections of distances between morphological landmarks to an explicitly geometric concept of shape characterized by the configuration of landmarks. We demonstrate this approach with a study of asymmetry in the wings of tsetse flies (Glossina palpalis gambiensis). The analysis revealed significant fluctuating and directional asymmetry for shape as well as ample shape variation among individuals and between the offspring of young and old females. The morphological landmarks differed markedly in their degree of variability but multivariate patterns of landmark covariation identified by principal component analysis were generally similar between fluctuating asymmetry (within-individual variability) and variation among individuals. Therefore there is no evidence that special developmental processes control fluctuating asymmetry. We relate some of the morphometric patterns to processes known to be involved in the development of fly wings.     

Fluctuating asymmetry and stress in a medieval Nubian population

Fluctuating asymmetry is commonly used as a bioindicator of developmental stress. This study addresses asymmetry under nutritional/systemic stress in the human craniofacial skeleton and its utility as an indicator of developmental instability. Crania from the diachronic Christian cemeteries at Kulubnarti (Sudanese Nubia) were chosen as a model for nutrition/systemic stress. Previous studies indicate that individuals from the Early Christian cemetery were subjected to greater developmental stress when compared with individuals from the Late Christian cemetery. Therefore, crania from the Early Christian cemetery should display a greater magnitude of fluctuating asymmetry than crania from the Late Christian cemetery. Thirty adult crania of comparable age and sex were selected from each population. Landmark coordinates were digitized in two separate trials and averaged to minimize error. Euclidean distance matrix analysis (EDMA) was used to measure and compare the magnitude of fluctuating asymmetry in each sample. Results indicate that crania from the Early Christian cemetery display greater amounts of fluctuating asymmetry than those from the Late Christian cemetery, as predicted. The degree of fluctuating asymmetry for each linear distance is highly correlated between the cemeteries, suggesting that all humans may share common patterns of fluctuating asymmetry in the skull. In contrast, there is little correlation between magnitude of fluctuating asymmetry and length of linear distance, between-subject variability, or measurement error. These results support the hypothesis that poor nutrition/systemic stress increases developmental instability in the human skull and that increased fluctuating asymmetry constitutes morphological evidence of this stress.     

Shaping intraspecific variation: Development,ecology and the evolution of morphology and life history variation in tiger salamanders

The tiger salamander,Ambystoma tigrinum, is a geographically widespread, morphologically variable, polytipic species. It is among the most variable species of salamanders in morphology and life history with two larval morphs (typical and cannibal) and three adult morphs (metamorphosed, typical branchiate, cannibal branchiate) that vary in frequency between subspecies and between populations within subspecies. We report morphometric evidence suggesting that branchiate cannibals arose through intraspecific change in the onset or timing of development resulting in the wider head and hypertrophied tooth-bearing skull bones characteristic of this phenotype. We also quantified bilateral symmetry of gill raker counts and abnormalities, then evaluated fluctuating asymmetry as a measure of the developmental stability of each morph. There was a significant interaction between fluctuating asymmetry of developmental abnormalities in cannibals and typicals and the locality where they were collected, suggesting that relative stability of each phenotype could vary among populations. While altered timing of developmental events appears to have a role in the evolution and maintenance of morphs, novel phenotypes persist only under favorable ecological conditions. Predictability of the aquatic habitat, genetic variation, kinship, body size, intraspecific competition and predation all affect expression and survival of the morphs inA. tigrinum. This taxon provides an excellent model for understanding the diversity and complexity of developmental and ecological variables controlling the evolution and maintenance of novel phenotypes.     

Host alkaloids differentially affect developmental stability and wing vein canalization in cactophilic Drosophila buzzatii

Host shifts cause drastic consequences on fitness in cactophilic species of Drosophila. It has been argued that changes in the nutritional values accompanying host shifts may elicit these fitness responses, but they may also reflect the presence of potentially toxic secondary compounds that affect resource quality. Recent studies reported that alkaloids extracted from the columnar cactus Trichocereus terscheckii are toxic for the developing larvae of Drosophila buzzatii. In this study, we tested the effect of artificial diets including increasing doses of host alkaloids on developmental stability and wing morphology in D. buzzatii. We found that alkaloids disrupt normal wing venation patterning and affect viability, wing size and fluctuating asymmetry, suggesting the involvement of stress–response mechanisms. Theoretical implications are discussed in the context of developmental stability, stress, fitness and their relationship with robustness, canalization and phenotypic plasticity.     

Fluctuating asymmetry and inbreeding in Scandinavian gray wolves (Canis lupus)

We investigated fluctuating asymmetry in 13 traits of the skulls and jaws of historical and contemporary populations of Scandinavian gray wolves (Canis lupus). We hypothesized that there is a higher level of fluctuating asymmetry in the inbred contemporary population than in the historical population. Our analyses did not detect any difference in the level of fluctuating asymmetry as predicted. We propose different explanation for this lack of change in fluctuating asymmetry. It is assumed that a large number of studies have failed to find a positive correlation between the level of genetic stress and developmental instability and have therefore never been published, which hampers a good understanding of fluctuating asymmetry as an indicator of developmental instability. The current study is thus important in this context. The gray wolf population in Scandinavia is characterized by an extreme bottleneck followed by two and a half decades of strong inbreeding, but no associated change in fluctuating asymmetry is detected.