Mandible asymmetry and genetic diversity in island populations of the common shrew, Sorex araneus

Mandibles from 13 island and six mainland populations of common shrews from the west coast of Scotland were subjected to geometric morphometric analysis in order to investigate the relationship between genetic diversity and fluctuating asymmetry. Although population mean shape fluctuating asymmetry (FA) and size FA were significantly inversely correlated with population genetic diversity this result was substantially due to one island. Sanda, the smallest island with by far the lowest genetic diversity, also had the highest FA. When Sanda was removed from the analysis, the relationship was not significant. There was no relationship between genetic diversity and FA at the individual level, whether measured as mean locus heterozygosity or d(2). In general, if genetic variation affects FA at all, the effect is weak and may only be of biological interest in very small populations.     

Quantifying asymmetry: Ratios and alternatives

Traditionally, the study of metric skeletal asymmetry has relied largely on univariate analyses, utilizing ratio transformations when the goal is comparing asymmetries in skeletal elements or populations of dissimilar dimensions. Under this approach, raw asymmetries are divided by a size marker, such as a bilateral average, in an attempt to produce size‐free asymmetry indices. Henceforth, this will be referred to as “controlling for size” (see Smith: Curr Anthropol 46 (2005) 249‐273). Ratios obtained in this manner often require further transformations to interpret the meaning and sources of asymmetry. This model frequently ignores the fundamental assumption of ratios: the relationship between the variables entered in the ratio must be isometric. Violations of this assumption can obscure existing asymmetries and render spurious results. In this study, we examined the performance of the classic indices in detecting and portraying the asymmetry patterns in four human appendicular bones and explored potential methodological alternatives. Examination of the ratio model revealed that it does not fulfill its intended goals in the bones examined, as the numerator and denominator are independent in all cases. The ratios also introduced strong biases in the comparisons between different elements and variables, generating spurious asymmetry patterns. Multivariate analyses strongly suggest that any transformation to control for overall size or variable range must be conducted before, rather than after, calculating the asymmetries. A combination of exploratory multivariate techniques, such as Principal Components Analysis, and confirmatory linear methods, such as regression and analysis of covariance, appear as a promising and powerful alternative to the use of ratios. Am J Phys Anthropol 154:498–511, 2014. © 2014 Wiley Periodicals, Inc.     

Dental arch asymmetry in an isolated Adriatic community

Developmental stability reflects the ability of a genotype to develop in the same way under varying environmental conditions. Deviations from developmental stability, arising from disruptive effects of environmental and genetic stresses, can be measured in terms of fluctuating asymmetry, a particularly sensitive indicator of the ability to cope with these stresses during ontogeny. In an inbred Adriatic island population, we expected dental arch fluctuating asymmetry 1) to be higher than in an outbred sample from the same island, and 2) within this population, to increase with the level of inbreeding. Due to environmental stress, we also expected to find higher fluctuating asymmetry in the outbred island population than in an urban reference group from the same country. The material consisted of 506 dental casts of 253 children from 1) the island of Hvar, and 2) Zagreb, Croatia. Three-dimensional coordinates of 26 landmarks spanning the arches were digitized. The analysis partitioned the asymmetry of arch forms into components for directional and fluctuating bilateral asymmetry, using the appropriate Procrustes method (geometric morphometrics). The results corroborated the hypotheses. Fluctuating asymmetry was found to be higher on the island than in Zagreb in all groups and in both jaws, and increased significantly with endogamy level in the lower jaw. There was no significant directional asymmetry in the Zagreb sample and likewise none in the upper jaws of the outbred island group, but significant directional asymmetry in both jaws of the inbred population and also in the lower jaws of the outbred island group. These results suggest an environmental as well as a genetic influence on dental arch asymmetry. Although the lower jaws expressed these two stresses almost additively, the upper jaws appeared to be better buffered. The role of directional asymmetry as a potential indicator of craniofacial developmental instability clearly merits further attention.     

Mixture analysis of asymmetry: modelling directional asymmetry, antisymmetry and heterogeneity in fluctuating asymmetry

The occurrence of different forms of asymmetry complicates the analysis and interpretation of patterns in asymmetry. Furthermore, between-individual heterogeneity in developmental stability (DS) and thus fluctuating asymmetry (FA), is required to find relationships between DS and other factors. Separating directional asymmetry (DA) and antisymmetry (AS) from real FA and understanding between-individual heterogeneity in FA is therefore crucial in the analysis and interpretation of patterns in asymmetry. In this paper we introduce and explore mixture analysis to (i) identify FA, DA and AS from the distribution of the signed asymmetry, and (ii) to model and quantify between-individual heterogeneity in developmental stability and FA. In addition, we expand mixtures to the estimation of the proportion of variation in the unsigned FA that can be attributed to between-individual heterogeneity in the presumed underlying developmental stability (the so-called hypothetical repeatability). Finally, we construct weighted normal probability plots to investigate the assumption of underlying normality of the different components. We specifically show that (i) model selection based on the likelihood ratio test has the potential to yield models that incorporate nearly all heterogeneity in FA; (ii) mixtures appear to be a powerful and sensitive statistical technique to identify the different forms of asymmetry; (iii) restricted measurement accuracy and the occurrence of many zero observations results in an overestimation of the hypothetical repeatability on the basis of the model parameters; and (iv) as judged from the high correlation coefficients of the normal probability plots, the underlying normality assumption appears to hold for the empirical data we analysed. In conclusion, mixtures provide a useful statistical tool to study patterns in asymmetry.     

Correspondence between enamel hypoplasia and odontometric bilateral asymmetry in Australian twins

Four aspects of enamel hypoplasia of the maxillary central incisor and mandibular canine (hypoplasia presence, width, cumulative width, and crown position) were correlated with directional and fluctuating measures of bilateral odontometric asymmetry in a large panel (n = 950) of South Australian twins. Hypoplasia and asymmetry are thought to reflect general developmental disruption, but they show few correlations beyond the expected statistical type I error. This may relate to differences in their specific etiology, the composite nature of overall crown dimensions, a general lack of stress, and the extended period of formation of dental crowns. In contrast, asymmetry is marginally more detectable in a subsample separated according to hypoplastic teeth, suggesting that correspondence may be clearer in comparisons at the population rather than individual level. The most notable difference is the greater variability of asymmetry measures in hypoplastic individuals.     

Acid stress increases pelvic spine asymmetry in juvenile three-spined sticklebacks

In the evaluation of the effect of acidic water on the symmetrical development of the pelvic spines in juvenile three-spined sticklebacks Gasterosteus aculeatus , directional rather than fluctuating asymmetry was found, with left spines being, on average, longer than the right. Fish that were exposed for a period of c. 2 months to acidic pH levels grew significantly more asymmetrical pelvic spines than their control full-siblings held in unmanipulated water. Average spine size was not affected by the experimental treatment.     

Dermatoglyphic asymmetry and diversity in some pathologies

The evaluation of dermatoglyphic asymmetry represents a specific estimate of the stability of intrauterine development. In the present study, we analyzed the level of asymmetry and diversity in the radial and ulnar counts of each finger in 400 health Sardinian individuals and in 469 Sardinian subjects with four common diseases in Sardinia: type 1 diabetes, type 2 diabetes, arterial hypertension and multiple sclerosis. To measure the asymmetry, we used three indices: fluctuating asymmetry, the index of asymmetry and the index of diversity. The differences from the control group are only rarely significant. The values of fluctuating asymmetry do not present a particular distribution in relation to the pathologies, while the values of {ie139-1} and diversity are usually higher in the pathological groups. The differentiation is especially evident in the subjects with multiple sclerosis, intermediate in the diabetics and practically nil in the hypertense individuals.     

Heritability of directional and fluctuating asymmetry for mandibular characters in random-bred mice

In bilateral characters, two kinds of asymmetries are common: fluctuating asymmetry (FA), or nondirectional variation between left and right sides, and directional asymmetry (DA), in which one side is consistently larger than the other. FA has been extensively used as a measure of developmental stability because of its presumed environmental basis whereas DA has not typically been recommended because it has been presumed to have at least some genetic basis. To test these two hypotheses, heritabilities were calculated via parent–offspring regression for both DA and FA in 10 triply measured mandible characters in random-bred mice. Midparent estimates of heritabilities of DA in the 10 characters were quite low (mean = 0.06), but significant for one character as well as the sum of the DA values over all characters (0.21). Midparent estimates of heritability of FA in the 10 characters also were low (mean = 0.03), but not significant for any individual character or the sum of the FA values over all characters. Heritabilities of developmental stability calculated from heritabilities and repeatabilities of FA in the mandible characters were higher in magnitude (mean of midparent estimates = 0.45), but all still were not statistically significant. It was concluded that both hypotheses were supported, but that genetic variation in DA was so small that the potential for DA as an indicator of developmental stability should be explored.     

Genetics of wing size asymmetry in Drosophila buzzatii

Contemporary approaches that use fluctuating asymmetry (FA) as a possible target for natural and sexual selection are based on the premise that FA is a quantifiable expression of developmental instability (DI) that is inherited. Previous work with Drosophila buzzatii found that male mating success was correlated positively to body size (wing length) and negatively to FA, but these relationships seem to be environmentally induced. Heritability of FA was low and not significantly different from zero, but statistical power was also estimated to be very low and, hence, no conclusive evidence could be obtained. A large half‐sib mating design is used here to examine the relationships of different aspects of development for wing size. Consistently with previous findings, I found high heritabilities for wing length (WL) and wing width (WW), and positive correlations between both traits. Heritabilities of FA (FA_WL, FA_WW) were low (0.037) but significantly different from zero, and the genetic correlation between FA_WL and FA_WW was estimated as ?1 because the absolute value for the genetic covariance was similar in magnitude or even larger than the estimated genetic variances of both traits. This suggests that these two traits should be considered to be the same character. The between‐trait phenotypic correlation in FA, which reduces to the repeatability in this situation, was positive and statistically significant thus rendering an estimate of heritability for DI in D. buzzatii of . Nevertheless, the fact that left/right wing sizes were found to be determined by the same set of genes is difficult to reconcile with the presence of special genetic mechanisms that stabilize left/right development in this species. A qualitatively different pattern for asymmetry was observed when the nonlinear composite character wing area (WA ≈ WL × WW) was used, and . Although the results could be made compatible with the existence of a diallelic locus with antagonistic pleiotropic effects on FA_WL and FA_WW that combine multiplicatively to produce overdominance for FA_WA, the available evidence is extremely weak at best. Finally, a test to the null hypothesis of a nongenetic basis of FA, particularly relevant to those situations when directional asymmetry may be heritable, is suggested.     

Response of fluctuating and directional asymmetry to selection on wing shape in Drosophila melanogaster

We tested whether directional selection on an index-based wing character in Drosophila melanogaster affected developmental stability and patterns of directional asymmetry. We selected for both an increase (up selection) and a decrease (down selection) of the index value on the left wing and compared patterns of fluctuating and directional asymmetry in the selection index and other wing traits across selection lines. Changes in fluctuating asymmetry across selection lines were predominantly small, but we observed a tendency for fluctuating asymmetry to decrease in the up-selected lines in both replicates. Because changes in fluctuating asymmetry depended on the direction of selection, and were not related to changes in trait size, these results fail to support existing hypotheses linking directional selection and developmental stability. Selection also produced a pattern of directional asymmetry that was similar in all selected lines whatever the direction of selection. This result may be interpreted as a release of genetic variance in directional asymmetry under selection.     

The statistical analysis of fluctuating asymmetry: REML estimation of a mixed regression model

The unbiased estimation of fluctuating asymmetry (FA) requires independent repeated measurements on both sides. The statistical analysis of such data is currently performed by a two-way mixed ANOVA analysis. Although this approach produces unbiased estimates of FA, many studies do not utilize this method. This may be attributed in part to the fact that the complete analysis of FA is very cumbersome and cannot be performed automatically with standard statistical software. Therefore, further elaboration of the statistical tools to analyse FA should focus on the usefulness of the method, in order for the correct statistical approaches to be applied more regularly. In this paper we propose a mixed regression model with restricted maximum likelihood (REML) parameter estimation to model FA. This routine yields exactly the same estimates of FA as the two-way mixed ANOVA . Yet the advantages of this approach are that it allows (a) testing the statistical significance of FA, (b) modelling and testing heterogeneity in both FA and measurement error (ME) among samples, (c) testing for nonzero directional asymmetry and (d) obtaining unbiased estimates of individual FA levels. The switch from a mixed two-way ANOVA to a mixed regression model was made to avoid overparametrization. Two simulation studies are presented. The first shows that a previously proposed method to test the significance of FA is incorrect, contrary to our mixed regression approach. In the second simulation study we show that a traditionally applied measure of individual FA [abs(left – right)] is biased by ME. The proposed mixed regression method, however, produces unbiased estimates of individual FA after modelling heterogeneity in ME. The applicability of this method is illustrated with two analyses.     

On the adaptive accuracy of directional asymmetry in insect wing size

Subtle left-right biases are often observed in organisms with an overall bilateral symmetry. The evolutionary significance of these directional asymmetries remains uncertain, however, and scenarios of both developmental constraints and adaptation have been suggested. Reviewing the literature on asymmetry in insect wings, we analyze patterns of directional asymmetry in wing size to evaluate the possible adaptive significance of this character. We found that directional asymmetry in wing size is widespread among insects, with left- and right-biased asymmetries commonly observed. The direction of the asymmetry does not appear to be evolutionarily conserved above the species level. Overall, we argue that the very small magnitude of directional asymmetry, 0.7% of the wing size on average, associated with an extremely imprecise expression, precludes directional asymmetry from playing any major adaptive role.     

Morph‐dependent form of asymmetry in mandibles of the stag beetle Prosopocoilus inclinatus (Coleoptera: Lucanidae)

Abstract 1. The form of asymmetry in bilateral organs usually follows the same pattern within single populations. However, some exceptions may occur when a population consists of different phenotypes that are from different ontogenic backgrounds and under different selective pressures. We investigated the asymmetric patterns of mandibles of larvae, females, and males in the stag beetle Prosopocoilus inclinatus. 2. Larval mandibles exhibited directional asymmetry both in length and cross direction, whereas female mandibles showed directional asymmetry in cross direction. These asymmetric structures might be more effective in cutting wood fibres. 3. For the relation of male mandible length to body size, a model with a switch point showed a better fit to the data than a convex curve model. This shows that the males are dimorphic with two distinct morphs. 4. The form of asymmetry in male mandible length differed between the morphs. The smaller males exhibited left‐biased directional asymmetry in common with larvae, whereas the larger males exhibited fluctuating asymmetry. 5. This is a novel finding of a morph‐dependent asymmetry. The morph‐dependent asymmetry in males may be as a result of different selection on each morph or a developmental constraint from larval mandibles to adult ones.     

Interpopulation variation in fluctuating asymmetry of the palmar A-B ridge-count

Fluctuating asymmetry was measured by the Pearson correlation coefficient between a-b ridge-counts of the right and left hands. Such data were available for 38 samples, which were grouped by major geographical regions. Significant heterogeneity exists within some of the geographical groups but the between geographical group component is highly significant in both sexes. Our results show that a sizable fraction of variation in fluctuating asymmetry is related to geographical race. There is no evidence that it follows environmental or ecological lines. The variation between geographical races suggests that there is a genetic component in the magnitude of fluctuating asymmetry.     

Assemblage and population-level consequences of forest fragmentation on bilateral asymmetry in tropical montane birds

Habitat fragmentation has the potential to influence the development and thus the phenotype of organisms. The asymmetry of bilateral traits may be indicative of the extent to which developmental stability is compromised by the stressful conditions underlying fragmentation. Using an assemblage- and population-level approach, we explored asymmetry differences in tarsus and outermost tail feathers of birds inhabiting fragmented landscapes in the tropical Andes of Colombia. More than 2500 individuals of 185 species were mist-netted at nine forest sites representing continuous forest (> 1000 ha), medium- (70–110 ha), and small-sized (8–20 ha) fragments. Feathers showed true fluctuating asymmetry (FA), whereas tarsus presented a mixture of FA and directional asymmetry. Overall, asymmetry was lowest in continuous forest, and highest in small and medium fragments. These patterns remained unchanged when directionality and differences in species composition, abundance, and foraging tactics were considered. The population-level analyses showed a general trend of increased asymmetry variation in fragments, yet the responses were not always in the same direction. Increased asymmetry may represent an outcome of processes that contribute to the persistence of species in changing environments, and to the generation of phenotypic innovation, which suggests individual adjustments of development to deal with stress. This calls into question the deliberated application of FA as a biomonitoring tool for conservation.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 119–133.     

Dental asymmetry,maternal obesity,and smoking

This study examines the levels of fluctuating dental asymmetry in four samples of school children: those whose mothers were obese and had smoked during the pregnancy concerned (n = 111); those whose mothers were obese non-smokers (n = 114); those whose mothers were non-obese smokers (n = 104); and those whose mothers were lean non-smokers (n = 111). The degree of fluctuating asymmetry was assessed by means of a rescaled asymmetry measure. Obesity was defined as Quetelet's index in excess of 30, and smoking status as at least 20 cigarettes per day during the pregnancy concerned. When the magnitudes of fluctuating asymmetry in children of lean smokers were compared to the control group of lean non-smokers, no significant univariate differences were found. Children of obese mothers, whether these smoked or not, were found to have significantly raised levels of asymmetry. An analysis of variance confirmed that the combination of obesity and maternal smoking was a significant predictor of fluctuating dental asymmetry. The teeth involved tended to be the maxillary first incisor and molars. It is concluded that maternal obesity has a destabilizing effect on the developing fetus and that this effect appears to be enhanced in obese mothers who smoked. This effect was absent in lean mothers, irrespective of their smoking status. Am J Phys Anthropol 102:133–139. © 1997 Wiley-Liss, Inc.     

Effect of the 1990 die-off in the northern Italian seas on the developmental stability of the striped dolphin Stenella coeruleoalba (Meyen, 1833)

Developmental stability of the community of striped dolphins, Stenella coeruleoalba (Meyen, 1833), that died during the Mediterranean epizootic of 1990 was compared with that of the population prior to and after the epizootic, to assess whether animals that died were the developmentally less stable individuals in the population. Significantly higher levels of fluctuating asymmetry (FA) were found in those individuals that died. Tissue levels of organochlorine pesticide residues and PCBs were determined and the correlation between contaminant concentration and FA was tested. No correlations were found between the contaminant level and FA.