SIZE AND FLUCTUATING ASYMMETRY OF MORPHOMETRIC CHARACTERS IN MICE: THEIR ASSOCIATIONS WITH INBREEDING AND t-HAPLOTYPE

Abstract Fluctuating asymmetry (FA), a ubiquitous type of asymmetry of bilateral characters, often has been used as a measure of developmental instability in populations. FA is expected to increase in populations subjected to genetic stressors such as inbreeding or environmental stressors such as toxins or parasites, although results have not always been consistent. We tested whether FA in four skeletal size characters and mandible shape was greater in a population of wild‐derived mice reared in the laboratory and subjected to one generation of inbreeding (F = 0.25) versus that in an outbred group (F= 0.00). FA did not significantly differ between the inbred and outbred groups, despite the fact that these two groups differed dramatically in fitness under seminatural population conditions. As far as we know, this is the first study to evaluate the relationship between FA and inbreeding in wild house mice, and our general conclusion is opposite that of earlier work on laboratory inbred strains of mice and their hybrids. Size for two of the characters was significantly less in inbreds than in outbreds, however, and there was a significant difference between inbreds and outbreds in the signed differences of right and left sides in one character (humerus length). Some of the mice in both groups also were heterozygous or homozygous carriers of the t‐complex. Because mice carrying this chromosome 17 variant are known to have reduced fitness, we also tested whether they had greater FA than mice carrying non‐t‐haplotypes. The overall level of a composite FA index calculated from all four characters was in fact significantly higher in the t‐bearing mice. These combined results suggest that FA is not a generally sensitive proxy measure for fitness, but can be associated with fitness reductions for certain genetic stressors.     

Relationship between fluctuating asymmetry and fitness within and between stressed and unstressed populations of the wolf spider Pirata piraticus

Although developmental instability, measured as fluctuating asymmetry (FA), is expected to be positively related to stress and negatively to fitness, empirical evidence is often lacking or contradictory when patterns are compared at the population level. We demonstrate that two important properties of stressed populations may mask such relationships: (i) a stronger relationship between FA and fitness, resulting in stronger selection against low quality (i.e. developmental unstable) individuals and (ii) the evolution of adaptive responses to environmental stress. In an earlier study, we found female wolf spiders Pirata piraticus from metal exposed populations to be characterized by both reduced clutch masses and increased egg sizes, the latter indicating an adaptive response to stress. By studying the relationship between these two fitness related traits and levels of FA at individual level, we here show a significant negative correlation between FA and clutch mass in metal stressed populations but not in unstressed reference populations. As a result, levels of population FA may be biased downward under stressful conditions because of the selective removal of developmentally unstable (low quality) individuals. We further show that females that produced larger eggs in stressed populations exhibited lower individual FA levels. Such interaction between individual FA and fitness with stress may confound the effect of metal stress on FA, resulting in an absence of relationships between FA, fitness and stress at the population level.     

Geographical variation in asymmetry in Gasterosteus aculeatus

We tested whether fluctuating asymmetry (FA) in undisturbed populations is associated with several natural environmental factors and whether FA is negatively correlated with fitness in the wild. We compared the FA of multiple bony structural defences among 87 endemic populations of threespine stickleback ( Gasterosteus aculeatus L.) inhabiting pristine freshwater habitats on the islands of Haida Gwaii, British Columbia, Canada. Multi-trait FA for adults and juvenile fish varied extensively among populations, but only in adults did it correlate with geography and two habitat characteristics (pH and water colour). Mean FA among individual traits varied concordantly among populations but was not correlated within individuals. While asymmetrical fish showed slightly higher levels of parasitism as predicted, selection differentials based on age class comparisons suggested that asymmetrical fish had the same or marginally higher survival than symmetrical fish. Selection differentials of FA varied significantly among traits and may reflect variability in their functional importance and in the strength of selection on their developmental stability. The data imply that FA/fitness associations are heterogeneous and character-specific.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77 , 9–22.     

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.     

Evolution of faster development does not lead to greater fluctuating asymmetry of sternopleural bristle number inDrosophila

Both strong directional selection and faster development are thought to destabilize development, giving rise to greater fluctuating asymmetry (FA), although there is no strong empirical evidence supporting this assertion. We compared FA in sternopleural bristle number in four populations ofDrosophila melanogaster successfully selected for faster development from egg to adult, and in four control populations. The fraction of perfectly symmetric individuals was higher in the selected populations, whereas the FA levels did not differ significantly between selected and control populations, clearly indicating that directional selection for faster development has not led to increased FA in sternopleural bristle number in these populations. This may be because: (i) development time and FA are uncorrelated, (ii) faster development does result in FA, but selection has favoured developmentally stable individuals that can develop fast and still be symmetrical, or (iii) the increased fraction of symmetric individuals in the selected populations is an artifact of reduced body size. Although we cannot discriminate among these explanations, our results suggest that the relationship between development time, FA and fitness may be far more subtle than often thought.     

Is phenotypic canalization involved in the decline of the endemic Aquilegia thalictrifolia? Rethinking relationships between fluctuating asymmetry and species conservation status

Fluctuating asymmetry (FA), the deviation from the normal symmetrical condition of a morphological trait having specific morphological symmetry, increases in response to environmental and genetic stress, is related to phenotypic plasticity and is considered a tool for monitoring a species conservation status. However, FA–stress relations are dependent on measured traits or species‐specific characteristics such as mating system and habitat. This study investigates the relationships between FA, genetic diversity, population size, density and individual fitness traits (plant height, fruit and seed set), in the endemic Aquilegia thalictrifolia, a mixed breeder that is declining, but maintaining high levels of heterozygosity. Leaf and flower FA and other traits were investigated in 10 populations of A. thalictrifolia, the whole species range. As a result, we found similar patterns of FA in leaves and flowers between populations, indicating a homogenous level of stress between populations that differed for other traits. FA and the other traits were not related, including heterozygosity. Heterozygosity was not related to individual fitness traits with the exception of plant height. In accordance with other studies, we found that the role of FA as a tool for assessing the conservation status of a species or population should be reconsidered. However, we conclude that a low level of FA should not automatically be considered an indicator of good conservation status or low level of stress, because in species that evolved in highly stable environments it may indicate a scarce ability to plastically respond to environmental changes, as a consequence of environmental and genetic canalization. Further investigation of this point is needed.     

Habitat dependent associations between parasitism and fluctuating asymmetry among endemic stickleback populations

Inconsistencies in the relationship between fluctuating asymmetry (FA) and fitness may be due to selection acting on the degree of trait asymmetry that differs among populations or among traits. We assessed relationships between parasite susceptibility and fluctuating asymmetry in the number of bony lateral plates among 83 populations of freshwater Gasterosteus aculeatus (three spined stickleback) and among lateral plate positions that vary in the selection they experience for symmetry. The correlation between FA and parasite infection was highly variable among samples. Excess of infected asymmetric G. aculeatus increased significantly as the robustness of structural predator defences decreased. This effect was found for one parasite species only (Eustrongylides sp.) and was slightly stronger in females. In addition, there was a trend for there to be an excess of infected females asymmetric in those lateral plates positions that did not experience selection for their symmetry, although the trend only approached significance. These results suggest that selection for trait symmetry can obscure relationships between fitness and individual-wide developmental stability, providing one possible explanation for some of the heterogeneity in FA/fitness relationships seen in the literature. These results are also consistent with previous reports showing that ecological segregation between symmetric and asymmetric G. aculeatus and between sexes can alter the FA/fitness relationship.     

Fluctuating asymmetry and fitness correlations in two Engraulis encrasicolus populations

Correlations among several measures of fluctuating asymmetry (FA) and fitness‐related variables were assessed in two populations of the European anchovy Engraulis encrasicolus with fast growth (Aegean Sea) and slow growth (Ionian Sea), respectively. FA levels were borderline significantly higher in the Ionian than in the Aegean for some variables. Variation in otolith shape (deviation from population norm) was lower in the Ionian than the Aegean, contrary to expectation. Within the Aegean, there was no relation between any of the FA indexes and fitness estimators, while in the Ionian a composite otolith FA index was significantly negatively correlated to standard length at age only in 2 year‐old individuals. This difference between the Aegean and Ionian may have been related to the lower growth rate in the Ionian, as FA–fitness relations may be more apparent in less‐beneficial environments. The absence of significant correlations in the Aegean and the low correlation in one age group in the Ionian suggests that FA is not a sensitive indicator of individual fitness in adult E. encrasicolus.     

FLUCTUATING ASYMMETRY IS NONGENETICALLY RELATED TO MATING SUCCESS IN DROSOPHILA BUZZATII

Abstract To date, there is still no consensus on the real significance of fluctuating asymmetry (FA) in evolutionary biology. Some studies have established links between FA and Darwinian fitness, and in a number of cases intermediate heritabilities for FA have been reported. However, many claims have been raised against the generality of these findings. I therefore tested if FA of a sexually selected trait (wing length) is indeed related to male mating success in Drosophila buzzatii from field and laboratory samples and whether FA has detectable heritability. Single, unsuccessful males had greater asymmetry for wing length than their mating counterparts both in nature and under nonoptimal rearing environments, but the higher FA in single males is most likely due to a poorer average phenotypic condition because there was no evidence of a genetic basis for this trait. Further evidence of an increase in FA under larval food stress is suggested when comparing the magnitude of the FA levels between stressful and optimal environments. On methodological grounds, a linear model is suggested that allows directional asymmetry (DA) and any genetic variation of DA that may be present to be statistically eliminated from estimates of FA.     

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.     

Evolutionary history shapes the association between developmental instability and population‐level genetic variation in three‐spined sticklebacks

Developmental instability (DI) is the sensitivity of a developing trait to random noise and can be measured by degrees of directionally random asymmetry [fluctuating asymmetry (FA)]. FA has been shown to increase with loss of genetic variation and inbreeding as measures of genetic stress, but associations vary among studies. Directional selection and evolutionary change of traits have been hypothesized to increase the average levels of FA of these traits and to increase the association strength between FA and population‐level genetic variation. We test these two hypotheses in three‐spined stickleback (Gasterosteus aculeatus L.) populations that recently colonized the freshwater habitat. Some traits, like lateral bone plates, length of the pelvic spine, frontal gill rakers and eye size, evolved in response to selection regimes during colonization. Other traits, like distal gill rakers and number of pelvic fin rays, did not show such phenotypic shifts. Contrary to a priori predictions, average FA did not systematically increase in traits that were under presumed directional selection, and the increases observed in a few traits were likely to be attributable to other factors. However, traits under directional selection did show a weak but significantly stronger negative association between FA and selectively neutral genetic variation at the population level compared with the traits that did not show an evolutionary change during colonization. These results support our second prediction, providing evidence that selection history can shape associations between DI and population‐level genetic variation at neutral markers, which potentially reflect genetic stress. We argue that this might explain at least some of the observed heterogeneities in the patterns of asymmetry.     

Fluctuating Asymmetry in Body Traits Increases Predation Risks: Tawny Owl Selection Against Asymmetric Woodmice

During the last decade, the study of fluctuating asymmetry (FA) in relation to different fitness aspects has become a popular issue in evolutionary biology. There has been much recent debate in subtle departures from perfect symmetry in bilaterally paired morphological characters, and the extent to which such departure actually reflects aspects of individual quality and fitness. We used data from pellet collection and trapping sessions involving the trophic system Apodemus – Strix aluco, to test the hypothesis that asymmetric woodmice disproportionately fell prey to the tawny owl compared with “normal” woodmice. We found that woodmice preyed on by owls had significantly more asymmetric leg bones than survivors, particularly hind legs, those devoted to jumping. Thus asymmetry in locomotory traits apparently increased predation risks due probably to minor efficiency of asymmetric woodmice in evading predators or to their general low quality. These results suggest that FA affects fitness and consequently may be a good predictor of survival chances for woodmice, i.e. their quality; on the other hand, by removing asymmetric individuals, tawny owls can exert a stabilising selection on prey populations.Co-ordinating editor: M. Klaassen     

Individual asymmetry as a predictor of fitness in the bat Carollia perspicillata

The measurement of fitness in wild populations is a challenging task, and a number of proxies have been proposed with different degrees of success. Developmental instability/stability (DI) is an organismal property associated with variance in bilateral asymmetry (fluctuating asymmetry—FA) and a correlated effect on fitness. This study provides evidence to corroborate the hypothesis that asymmetry partly reflects DI and is correlated with a reduction in fitness measured by survival and reproduction in bats. We studied two colonies of the bat Carollia perspicillata in southeastern Brazil over 5 years, marking and recapturing individuals. Gaussian mixture models for signed Forearm Asymmetry (ForA) distribution indicated that ~20% of asymmetry variation was due to DI heterogeneity among individuals. ForA, body condition (Scaled Mass Index—SMI) and Forearm Length (ForL) were used as predictors of survival probability in Cormack‐Jolly‐Seber models. Asymmetry was negatively associated with survival, whereas SMI and ForL were positively associated. The male C. perspicillata defend sites within the roost that are favoured by female harems, but there are mating opportunities for bachelor males, leading to both territorial disputes and sperm competition. As predicted by sexual selection, ForA was negatively associated with relative Testicle Length, a measure of reproductive potential. In females, ForA was negatively associated with the probability of two pregnancies (as opposed to one) in a given breeding season. The effect magnitudes and directions of associations suggest that asymmetry, even though not perfectly reflecting DI variation, is a useful predictor for fitness components in C. perspicillata.     

Asymmetry and fitness in female yellow dung flies

Fluctuating asymmetry (FA) has been widely used as a measure of developmental stability, and two recent meta-analyses suggest FA may be associated with several fitness components, including fecundity, growth rate and longevity. However, these studies have been strongly criticised on a number of grounds, and it was suggested that further evidence was required before the importance of any associations could be accurately assessed. Furthermore, studies should be of individual FA and fitness components. Here we investigated associations between individual FA of the mid and hind tibia and several fitness related traits (including fecundity, fertility, longevity and offspring development time) in female yellow dung flies ( Scathophaga stercoraria ). As in several previous studies, asymmetry could be discerned from measurement error and was FA. However, we found no significant associations between any measure of FA and any fitness component regardless of how the data were analysed. Our results therefore do not support any fitness–FA association and suggest that as with other aspects of FA, associations may be trait and species specific.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 76 , 557–563.     

DEVELOPMENTAL STABILITY,FITNESS, AND TRAIT SIZE IN LABORATORY HYBRIDS BETWEEN EUROPEAN SUBSPECIES OF THE HOUSE MOUSE

The effects of hybridization on developmental stability and size of tooth characters were investigated in intersubspecific crosses between random-bred wild strains of the house mouse (Mus musculus domesticus and M. m. musculus). Fluctuating asymmetry (FA) and trait size were compared within and between parental, F₁, backcross, and F₂ hybrid groups. The relationship between FA and reproductive fitness within the F₁ hybrids was also studied. The results indicated that both FA and character size levels differed significantly between the two subspecies. The F₁ hybrids and the recombined groups (backcrosses and F₂ hybrids) showed heterosis for both parameters. No significant differences in the FA of fertile and sterile F₁ hybrid individuals were found. Comparison of the FA levels obtained in this study with those found in wild populations from the hybrid zone in Denmark showed that the levels of FA were lower in laboratory-bred samples than in the wild populations. This study provides further evidence that, in hybrids, the developmental processes underlying most of the morphological traits we studied benefit from a heterotic effect, despite the genomic incompatibilities between the two European house mice revealed by previous genetical and parasitological studies.     

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.     

Morphological variability and developmental instability in subpopulations of the Eurasian badger (Meles meles) in Denmark

Aim Local populations from different geographical regions may differ in the selection regimes to which they are exposed. Differences in environmental factors and population density may affect the relative importance of different selective forces (e.g. natural vs. sexual selection). We suggest a direction of investigation concerned with the developmental instability of morphological traits. The goal is to disclose putative small‐scale geographical differences in the evolutionary forces, which may be hard to detect. Location Craniometrical investigations were carried out on ninety‐eight skulls and teeth of the Eurasian badger (Meles meles) collected during the period 1995–97 from three different populations in Denmark. One of these thrives at low population density, whereas the two others are characterized by high local density. Methods The skulls were investigated for developmental instability (DI) using fluctuating asymmetry (FA) as its estimator. FA was measured on canines, molars, premolar teeth and other skull and mandible traits. For the statistical analyses, we applied nonparametric permutation tests. Results Evidence was found suggesting differentiation among populations in mean degree of FA, and the FA values measured on canines were higher in the high‐density populations. FA of the canines was significantly higher in males than females, in contrast to FA of the other traits. Evidence of a negative relationship between canine size and their FA was found, whereas no significant correlations were found between the molar and premolar teeth measures and their FA. Main conclusions Our results suggest that canines could be under directional selection stemming from intrasexual competition, which may be stronger in high‐density zones. The other teeth investigated seem to be under a stabilizing regime hence their FA is mainly affected by environmental stresses. The negative relationship between canine size and FA found in males suggests the capacity of badgers to respond in an evolutionary way to environmental changes, despite the low genetic variability previously found at the molecular level.     

SPONTANEOUS MUTATION PARAMETERS FOR ARABIDOPSIS THALIANA MEASURED IN THE WILD

Mutations are the ultimate source of genetic diversity and their contributions to evolutionary process depend critically on their rate and their effects on traits, notably fitness. Mutation rate and mutation effect can be measured simultaneously through the use of mutation accumulation lines, and previous mutation accumulation studies measuring these parameters have been performed in laboratory conditions. However, estimation of mutation parameters for fitness in wild populations requires assays in environments where mutations are exposed to natural selection and natural environmental variation. Here we quantify mutation parameters in both the wild and greenhouse environments using 100 25th generation Arabidopsis thaliana mutation accumulation lines. We found significantly greater mutational variance and a higher mutation rate for fitness under field conditions relative to greenhouse conditions. However, our field estimates were low when scaled to natural environmental variation. Many of the mutation accumulation lines have increased fitness, counter to the expectation that nearly all mutations decrease fitness. A high mutation rate and a low mutational contribution to phenotypic variation may explain observed levels of natural genetic variation. Our findings indicate that mutation parameters are not fixed, but are variables whose values may reflect the specific environment in which mutations are tested.     

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.     

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.