Problems of sampling and inference in the study of fluctuating dental asymmetry

Randomly distributed or “fluctuating” dental asymmetry has been accorded evolutionary meaning and interpreted as a result of environmental stress. However, except for congenital malformation syndromes, the determinants of human crown size asymmetry are still equivocal. Both a computer simulated sampling experiment using a combined sample size of N = 3000, and the requirements of adequate statistical power show that sample sizes of several hundred are needed to detect population differences in dental asymmetry. Using the largest available sample of children with defined prenatal stresses, we are unable to find systematic increases in crown size asymmetry. Given sampling limitations and the current inability to link increased human dental asymmetry to defined prenatal stresses, we suggest that fluctuating dental asymmetry is not yet established as a useful and reliable measure of general stress in human populations.     

Enamel hypoplasia in sympatric chimpanzee and gorilla

The prevalence of enamel hypoplasia in 229Pan andGorilla, from the Republic of Cameroon, is described. A substantially higher proportion of gorillas (76%) than chimpanzees (58%) was affected. The incidence of enamel hypoplasia was not a function of sex, body size, or pathology. A study of tooth formation, from radiographs of a further series of immature apes, indicated that the mandibular canine bore 99% of all information about hypoplasia events. In both species a marked regularity of hypoplastic grooving with an interval of about 11.4% of canine crown height was observed. This appears to reflect a semi-annual cycle of stress which is tentatively linked to the twice-yearly rainy season. Uniform spacing of hypoplastic grooves has been observed in a variety of fossil hominids. Readily observable hypoplastic time markers in the teeth have potential for disclosing growth rates in early Hominidae. This is considered important because of the profound significance which prolonged maturation and longevity characteristic of recent human beings have for the transmission of learned behavior and social bonding.     

Asymmetry of Early Paleozoic trilobites

Asymmetry in fossils can arise through a variety of biological and geological mechanisms. If geological sources of asymmetry can be minimized or factored out, it might be possible to assess biological sources of asymmetry. Fluctuating asymmetry (FA), a general measure of developmental precision, is documented for nine species of lower Paleozoic trilobites. Taphonomic analyses suggest that the populations studied for each taxon span relatively short time intervals that are approximately equal in duration. Tectonic deformation may have affected the specimens studied, since deviations from normal distributions are common. Several measures of FA were applied to 3–5 homologous measures in each taxon. Measurement error was assessed by the analysis of variance (ANOVA) for repeated measurements of individual specimens and by analysis of the statistical moments of the distributions of asymmetry measures. Measurement error was significantly smaller than the difference between measures taken on each side of a specimen. However, the distribution of differences between sides often deviated from a mean of zero, or was skewed or kurtosic. Regression of levels of FA against geologic age revealed no statistically significant changes in levels of asymmetry through time. Geological and taphonomic effects make it difficult to identify asymmetry due to biological factors. Although fluctuating asymmetry is a function of both intrinsic and extrinsic factors, the results suggest that early Cambrian trilobites possessed genetic or developmental mechanisms used to maintain developmental stability comparable to those of younger trilobites. Although the measures are biased by time averaging and deviations from the normal distribution, these data do not lend strong support to 'genomic' hypotheses that have been suggested to control the tempo of the Cambrian radiation.     

Developmental instability in Brassica campestris (Cruciferae): fluctuating asymmetry of foliar and floral traits

The degree of fluctuating asymmetry of bilateral traits provides a measure of developmental instability, which can be influenced by genetic as well as environmental stress. We studied genetic variation between and within two populations of the mustard Brassica campestris for asymmetry of foliar (cotyledon width) and floral (petal length and width) traits as well as for phenological (germination and flowering) and performance (biomass and flowering) traits. The two populations differed in mean expression of most traits, including asymmetry. However, within-population estimates of genetic variability tended to be lower for asymmetry than other traits. Asymmetry was greater in the population that had lower biomass accumulation and flower production, which supports the idea that population-level asymmetry may be indicative of population-level performance. However, within each population, evidence that performance was negatively correlated with asymmetry was equivocal. Within populations there was little or no concordance among estimates of asymmetry based on different structures, i.e., plants that had highly asymmetrical cotyledons did not tend to have highly asymmetrical petals. The lack of a general buffering capacity at the individual level may be explained by developmental processes (e.g., action of different genes or morphogens) as well as evolutionary processes (e.g., selection on asymmetry of different traits).     

Flower and cotyledon asymmetry in Brassica cretica: genetic variation and relationships with fitness

Plants of the partially self-incompatible perennial herb Brassica cretica, derived from controlled cross- and self-pollinations within each of seven populations, were raised under uniform conditions and scored for two measures of developmental stability, flower asymmetry (quantified as the difference in length and width between opposite petals) and cotyledon asymmetry (quantified as the difference in the area of the two lobes of each cotyledon). The primary goals were to assess the level of heritable variation in asymmetry, the effect of selfing on mean asymmetry, and the relationship between asymmetry and components of fitness. A paternal half-sibling analysis of data on flower asymmetry failed to detect significant levels of genetic variation at the within-population level, whereas the between-population component reached significance for all measures of asymmetry. Analysis of family-structured data from another crossing experiment revealed significant between-population variation in cotyledon asymmetry and a tendency for inbred progeny to produce more asymmetric cotyledons than outbred progeny. However, the response to inbreeding was weak and differed in magnitude between populations. Judging from the ranking of populations, we found no support for the hypothesis that the mean expression of developmental stability is controlled by genomewide characteristics such as the level of inbreeding. Correlations between measures of asymmetry and fitness were too low to be declared statistically or biologically significant. The present study provides little evidence that flower and cotyledon asymmetry serve as more appropriate predictors of genetic health than conventional (direct) measures of fitness.     

Trait variability and stress: canalization, developmental stability and the need for a broad approach

Trait variability (particularly fluctuating asymmetry) may provide a general measure of environmental stress applicable across taxa but consistent empirical support is lacking. Historically, stress effects were considered to act independently on trait canalization, developmental noise and trait size. However, in trait comparisons these processes are often assumed to be associated. Here we reconsider this issue and implications for detecting stress effects using trait variability. Published studies that consider multiple environments report little association between the effects of environmental variation on trait canalization and on developmental noise measured as fluctuating asymmetry, sug-gesting that environmental effects often act independently on these processes. To further test the usefulness of trait variability as an indicator of stress, comparisons across environ-ments should take a broad approach and report on several measures of trait variability, rather than focusing on only one index of fluctuating asymmetry as is commonly done.     

Relationship of enamel hypoplasia to the pattern of tooth crown growth: A discussion

The defects of enamel hypoplasia can be related to the layered structure of enamel which represents the sequence of development in tooth crowns. From such studies, it is possible to see that furrow-type enamel defects (the most common form of hypoplasia seen with the naked eye) are just the most prominent expression of a continuum which extends ever smaller, down to a microscopic disturbance to a single layer in the crown formation sequence. Furthermore, the progressive decrease in spacing between development layers which occurs down the crown sides, from occlusal to cervical, affects both the prominence and apparent width of the defects. This makes it difficult to use measurements as a means of estimating the duration of the disturbance causing a particular defect. The difficulty is even greater for the less common pitted or exposed-plane-type defects, for which the apparent width bears very little relationship with the duration of the growth disturbance. The defects of enamel hypoplasia can therefore be understood clearly only when examined under the microscope in relation to the structures which mark the development sequence of the tooth crown. Am J Phys Anthropol 104:89–103, 1997. © 1997 Wiley-Liss, Inc.     

Factors affecting the distribution of enamel hypoplasias within the human permanent dentition

Frequencies and morphological and chronological distributions of enamel hypoplasias are presented by tooth type (permanent I1 to M2s), based on a sample of 30 prehistoric Amerindians with complete and unworn dentitions. There is nearly a tenfold variation in frequency of defects by tooth, ranging from 0.13 per mandibular second molar to 1.27 per maxillary central incisor. The six anterior teeth average between 0.70 and 1.27 defects/tooth, whereas the eight posterior teeth average between 0.43 and 0.13 defects/tooth. Earlier developing teeth, such as incisors, have earlier peak frequencies of defects (2.0-2.5 years), while later developing teeth, such as second molars, have subsequent peak frequencies (5.0-6.0 years). These variations are relevant when comparing hypoplasia data based on different teeth. Differences in hypoplasia frequencies among teeth are not solely due to variation in time of crown development, as is usually reported. Rather, there is evidence for biological gradients in susceptibility to ameloblastic disruption. Anterior teeth are more hypoplastic than posterior teeth. More developmentally stable "polar" teeth are more hypoplastic than surrounding teeth. Polar teeth may be more susceptible to hypoplasias because their developmental timing is less easily disrupted. In all teeth, hypoplasias are most common in the middle and cervical thirds. Crown development and morphological factors, such as enamel prism length and direction, may influence the development and expression of enamel surface defects.     

Anterior thoracic hypoplasia: a separate entity from Poland syndrome

SUMMARY: Women presenting with anterior thoracic depression, breast hypoplasia, and subsequent asymmetry are often diagnosed with Poland syndrome regardless of pectoralis involvement, or are placed in the generic category of breast asymmetry or skeletal dysplasias. Recently, though, the term "sunken chest" has been used to describe forms of chest wall depression that previously may have fallen under generic skeletal dysplasias. The authors believe that, combined with hypoplasia of the ipsilateral breast, superior location of the nipple-areola complex compared with the contralateral side, and normal pectoralis muscles, this represents a previously undefined and real condition called anterior thoracic hypoplasia. During the past 4 years, the authors have treated eight women who have presented with a diagnosis of Poland syndrome or pectus excavatum, all of whom share the same characteristics-unilateral sunken anterior chest wall, hypoplasia of the breast, superiorly placed nipple-areola complex, normal pectoralis muscle, and normal sternal position. All of the patients underwent correction of breast asymmetry and unilateral anterior thoracic hypoplasia with augmentation mammaplasty, a method that when tailored for each side yields good aesthetic results. The average age of the patients was 31 years and the average chest size was 34. Cup size, as measured by the patient's standard bra, was a B on the nonaffected side in all patients and an A on the affected side in all patients except one. Of the eight patients, seven had the right anterior chest and breast involved, whereas one patient had involvement on the left. For all of the patients, the nipple and areola of the hypoplastic side were smaller and in a more superior position compared with the contralateral side on visual inspection. In the eight patients, a total of 19 augmentations (15 primary augmentations and four revisions) and one mastopexy were performed. Ten inframammary-fold approaches and nine periareolar approaches were used, and all of the implants were placed in a partial submuscular position, except for two implants placed in a subglandular position that were converted to partial submuscular positions in a secondary setting. In all the women, the sternal head of the pectoralis muscle was present and the pectoralis muscle appeared to be equal in size compared to the contralateral side. Nine different types of implants were used. Average implant fill volume measured 412 cc on the hypoplastic side and 257 cc on the contralateral side. In follow-up, all of the patients were satisfied with their operation and rated their aesthetic outcome as very good to excellent. The authors believe that anterior thoracic hypoplasia is a real, previously misdiagnosed and undescribed condition, and that both chest wall and breast deformities can be corrected safely and with excellent results using proper augmentation planning and implant selection.     

Fluctuating dental asymmetry: Variation among skeletal populations

Recent investigations have shown that nongenetic, environmental factors can adversely affect dental growth and produce bilateral asymmetries in tooth size. When asymmetries do not favor either side, i.e., absence of directional asymmetry, the condition is termed fluctuating asymmetry. Fluctuating asymmetry of the mesiodistal and buccolingual dimensions of the total permanent dentition was compared among human skeletal populations which differ socio-economically and nutritionally. Odontometric data were collected from prehistoric hunters (Indian Knoll site), later aboriginal farming groups (Campbell and Larson sites), and a modern cadaver population (Hamann-Todd). The magnitude of asymmetry is expressed by the familiar correlation coefficient, r. The proportion, then, of intra-individual variation due to fluctuating asymmetry is equal to 1-r. With Wilcoxon's signed ranks test on the correlation coefficients no significant sex difference was shown within populations. Among groups, though, Indian Knoll was the most odontometrically asymmetrical; moreover, within Indian Knoll, the taller and ostensibly better nourished individuals had larger, less asymmetrical teeth than the shorter individuals. These results suggest that environmentally mediated growth disturbance may be sensitively reflected by dental asymmetry. A population exhibiting other signs of severe growth disturbance, e.g., enamel hypoplasia and Harris lines, was the most dentally asymmetrical.     

Developmental correlates of crown component asymmetry and occlusal discrepancy

To improve our understanding of dental asymmetry, more anatomically discriminating measurements than maximum crown dimensions were used. The relation between antimeres and opponents in permanent first molar teeth of 192 twins were studied with respect to crown component measures. Several statistical methods were used to describe asymmetry and discrepancy of occluding units to correlate with developmental stress indicators such as zygosity, birth weight, and congenital disease. To varying degrees, developmental correlates are found to be associated with asymmetry. The amount of occlusal discrepancy seems to be a direct function of bilateral asymmetry. Heterogeneity of MZ-DZ total (among plus within pair) variances occurs fairly consistently for asymmetry but not for discrepancy, implying differential environmental influences between zygosities regarding asymmetry. Genetic variance estimates, designed to be unbiased by differences in environmental variances, are significant for cusp size but not for asymmetry. Our results suggest that asymmetry at the individual cusp level may be an indicator of developmental disruption and that environmental effects, particularly prenatal, may be greater for antimeric units than for occluding units.     

Genetic and environmental influences on bilateral dental asymmetry in Northwest Indian twins

The role of genetic and environmental factors on dental asymmetry (in maximum crown dimensions) was examined using 58 pairs of twins (23 MZ and 35 DZ) from Chandigarh, India. The t'-test for equality of means by zygosity showed only one variable significantly different among 56: this is ascribable to Type 1 error. Heterogeneity of MZ-DZ total variance was observed in 42.9% of traits of the two types (fluctuating and directional) of bilateral asymmetry. In general, MZ twins showed higher total variance than DZ pairs. MZ twins also showed stronger environmental covariance for a majority of the traits. Dental asymmetry measures thus yielded consistently low genetic variance ratios and indicated predominantly complex environmental determinism. Since fluctuating asymmetry is widely believed to be an environmental stress indicator, this data set allows confirmation of methods for detecting unequal environmental influences on the zygosities which bias estimates of genetic variance and heritability.     

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.     

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.     

The influence of wind on spiral grain formation in conifer trees

The correlation between spiral grain formation and crown asymmetry was investigated in 18 Scots pine (Pinus sylvestris L.) and 17 Norway spruce [Picea abies (L.) Karst.] trees selected from clones of each species growing in the south of Sweden. The angle between the longitudinal direction of the tracheids in the outermost year ring compared to the longitudinal direction of the stem was measured by scribing lines which followed the direction of the tracheids. The crown asymmetry was measured by taking photographs of the trees followed by a simple picture analysis of the tree. Wind data for the growing seasons of 1997 and 1998 were obtained from the Swedish Meteorological and Hydrological Institute. The results showed a significant correlation between the angle of the tracheids compared to the stem longitudinal direction going from a left-handed angle if the trees had a crown projected to the north towards a right-handed angle the more the crown projects to the south. Received: 6 September 1999 / Accepted: 20 January 2000     

Peristalsis of airway smooth muscle is developmentally regulated and uncoupled from hypoplastic lung growth

Prenatal airway smooth muscle (ASM) peristalsis appears coupled to lung growth. Moreover, ASM progenitors produce fibroblast growth factor-10 (FGF-10) for lung morphogenesis. Congenital diaphragmatic hernia (CDH) is associated with lung hypoplasia, FGF-10 deficiency, and postnatal ASM dysfunction. We hypothesized ASM dysfunction emerges in tandem with, and may contribute toward, the primordial lung hypoplasia that precedes experimental CDH. Spatial origin and frequency of ASM peristaltic waves were measured in normal and hypoplastic rat lungs cultured from day 13.5 of gestation (lung hypoplasia was generated by nitrofen dosing of pregnant dams). Longitudinal lung growth was assayed by bud counts and tracing photomicrographs of cultures. Coupling of lung growth and peristalsis was tested by stimulation studies using serum, FGF-10, or nicotine and inhibition studies with nifedipine or U0126 (MEK1/2 inhibitor). In normal lung, ASM peristalsis is developmentally regulated: proximal ASM becomes quiescent (while retaining capacity for cholinergic-stimulated peristalsis). However, in hypoplastic lung, spontaneous proximal ASM activity persists. FGF-10 corrects this aberrant ASM activity in tandem with improved growth. Stimulation and inhibition studies showed that, unlike normal lung, changes in growth or peristalsis are not consistently accompanied by parallel modulation of the other. ASM peristalsis undergoes FGF-10-regulated spatiotemporal development coupled to lung growth: this process is disrupted early in lung hypoplasia. ASM dysfunction emerges in tandem with and may therefore contribute toward lung hypoplasia in CDH.     

Fluctuating dental asymmetry: A measure of developmental instability in Down syndrome

Subjects with Down syndrome provide a useful model for investigating the effect of chromosomal aneuploidy on developmental pathways. Studies suggest that a major effect of trisomy is a decrease in developmental stability. The present study examines fluctuating dental asymmetry in Down syndrome. Mesiodistal crown diameters were measured from dental casts of 114 Down syndrome subjects. Correlation coefficients for antimeric permanent teeth served as an index of dental asymmetry. These values were compared with normal values obtained from the literature. Fluctuating dental asymmetry is thought to reflect the relative success of developmental homeostasis in countering developmental disturbances. Down syndrome subjects have significantly increased dental asymmetry. In addition, they show a disproportionate increase in dental asymmetry for those teeth reported to have the least developmental stability. These results support the contention that the chromosomal imbalance in Down syndrome results in amplified developmental instability.     

Tall men with medium body fat mass percentage display more developmental stability

A symmetrical body may signal the ability of an individual to cope with developmental perturbations and may thus be considered a ‘health certificate’. It is known that symmetrical men are considered more attractive by women and that their reproductive success is higher. This study examined the associations between measures of body structure and fluctuating asymmetry in young Turkish men. Weight, height, and bioelectrical impedance were measured in a sample of 250 men residing in Ankara (mean age = 18.4, SD = 0.6), and body mass index was calculated. Fluctuating asymmetry was measured using hand length, hand width, elbow width, wrist width, knee width, ankle width, foot length, foot width, ear length, and ear width. According to the obtained findings, there is a negative linear relationship between composite fluctuating asymmetry (CFA) and height, and a positive quadratic relationship between CFA and fat mass. These results might indicate that the tall Turkish men with medium body fat mass percentage display more developmental stability.     

SHIFTS IN BILATERAL ASYMMETRY WITHIN A DISTRIBUTION RANGE: THE CASE OF THE CHUKAR PARTRIDGE

Abstract Three major types of bilateral asymmetry (fluctuating asymmetry, directional asymmetry, and antisymmetry) have long been recognized in the literature. Little, however, is known about transitions between asymmetry types, especially in natural populations. It is often assumed that directional asymmetry and antisymmetry have a larger genetic basis than fluctuating asymmetry. This leads many scientists to exclude traits or populations showing either directional asymmetry or antisymmetry from developmental instability studies, focusing attention on fluctuating asymmetry alone. This procedure may bias the findings and thus our understanding of patterns of bilateral asymmetry and the factors influencing it. To examine changes in bilateral asymmetry across the distribution range of a species, I studied the length of the third toe in 11 chukar partridge (Alectoris chukar) populations across a steep environmental gradient of 320 km within the species' range in Israel. This trait was selected due to its adaptive value in the chukar, a species that spends much of its activity walking, and due to its high measurement repeatability. Moving from the core toward the very extreme periphery of the range, the following four trends are detected: (1) the expression of the directional asymmetry component significantly increases; (2) the frequency of symmetrical individuals in the population significantly decreases, with a sharp decline at the steepest part of the climatic and environmental gradient studied, within the Mediterranean‐desert ecotone; (3) mean asymmetry levels, as estimated using the unsigned difference between the right and left toe, significantly increases; and (4) the range of asymmetry increases such that the most asymmetrical individuals originate from the very edge of the range. These findings provide primary evidence that substantial shifts in asymmetry may occur across short geographical distances within a species' distribution range. They show a continuum between asymmetry types and support the notion that all three types of asymmetry can reflect developmental instability. Further studies of developmental instability should be designed so that they enable detection of transitions between asymmetry types across natural populations. Such a procedure may partly resolve some of the contradictions seen in the literature regarding the relationship between bilateral asymmetry and environmental stress.     

Sex and asymmetry in humans: what is the role of developmental instability?

Because asymmetric individuals are less attractive and may suffer from reduced fitness, bilateral asymmetry is widely believed to affect human sexual selection. Its evolutionary significance is based on the presumed relationship with developmental instability (DI). Yet, relationships between DI and bilateral asymmetry are often weak and possibly confounded by asymmetric mechanical loadings because of handedness. We related asymmetry in hands and faces to degrees of handedness and sexual behaviour in 100 humans. Handedness correlated to levels of asymmetry, thereby likely invalidating the use of asymmetry to estimate DI. For facial asymmetry, applying existing theoretical models refuted a link between asymmetry and DI. Explicit statistical modelling at the level of DI confirmed the absence of a link between DI and aspects of sexual behaviour. Nevertheless, asymmetries in both hands and face correlated significantly with sexual behaviour. We conclude that bilateral asymmetry per se, rather than its presumed link with DI, more likely relates to measures of human sexual behaviour. Because lateralization of behaviour appears widespread, evaluating the role of DI in evolution and ecology relies on a very critical selection of traits whose asymmetry can reliably reflect DI.