DEVELOPMENTAL STABILITY IN LEAVES OF CLARKIA TEMBLORIENSIS (ONAGRACEAE) AS RELATED TO POPULATION OUTCROSSING RATES AND HETEROZYGOSITY

Four natural populations of Clarkia tembloriensis, whose levels of heterozygosity and rates of outcrossing were previously found to be correlated, are examined for developmental instability in their leaves. From the northern end of the species range, we compare a predominantly selfing population (t? = 0.26) with a more outcrossed population (t? = 0.84), which is genetically similar. From the southern end of the range, we compare a highly selfing population (t? = 0.03) with a more outcrossed population (t? = 0.58). We measured developmental stability in the populations using two measures of within-plant variation in leaf length as well as calculations of fluctuating asymmetry (FA) for several leaf traits. Growth-chamber experiments show that selfing populations are significantly more variable in leaf length than more outcrossed populations. Developmental instability can contribute to this difference in population-level variance. Plants from more homozygous populations tend to have greater within-plant variance over developmentally comparable nodes than plants from more heterozygous populations, but the difference is not significant. At the upper nodes of the plant, mature leaf length declines steadily with plant age, allowing for a regression of leaf length on node. On average, the plants from more homozygous populations showed higher variance about the regression (MSE) and lower R² values, suggesting that the decline in leaf length with plant age is less stable in plants from selfing populations than in plants from outcrossing populations. Fluctuating asymmetry (FA) was calculated for four traits within single leaves at up to five nodes per plant. At the early nodes of the plant where leaf arrangement is opposite, FA was also calculated for the same traits between opposite leaves at a node. Fluctuating asymmetry is significantly greater in the southern selfing population than in the neighboring outcrossed population. Northern populations do not differ in FA. Fluctuating asymmetry can vary significantly between nodes. The FA values of different leaf traits were not correlated. We show that developmental stability can be measured in plants using FA and within-plant variance. Our data suggest that large differences in breeding system are associated with differences in stability, with more inbred populations being the least stable.     

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.     

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.     

Developmental stability in hybrids between the sibling species pair,Drosophila melanogaster and Drosophila simulans

Drosophila melanogaster and its sibling species D. simulans were hybridized in the laboratory to test the hypothesis that developmental homeostasis in hybrids between two species having no prior gene flow would be significantly reduced. Developmental stability was assessed by measuring fluctuating asymmetry for three bilateral traits: sternopleural chaetae, wing length, and fronto-orbital plus frontal chaetae. Male F₁ hybrids showed no decrease in developmental stability compared to males of parental species. Female hybrids showed significant fluctuating asymmetry compared to other flies. The results are discussed with respect to ideas about coadaptation and gene flow based upon previous studies of hybrid developmental stability.     

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.     

INHERITANCE OF MERISTIC VARIATION AND THE EVOLUTION OF DEVELOPMENTAL STABILITY IN RAINBOW TROUT

We found relatively high heritabilities in the narrow sense for seven of eight meristic characters in a population of rainbow trout using regression of mean progeny values on mid-parent values. In sharp contrast, there is no statistically significant additive genetic variance controlling developmental stability, as measured by fluctuating asymmetry (h² = 0.02). However, there is a significant correlation between the average heterozygosity of each family at isozyme loci and the average number of asymmetric traits per individual. We have previously reported a strong correlation between heterozygosity at protein loci and decreased fluctuating asymmetry in this and other salmonid populations. Thus, there is little or no additive, but substantial dominance, genetic variation affecting fluctuating asymmetry. This suggests that there has been directional selection for increased developmental stability.     

Patterns of leaf asymmetry changes in Plantago major L. (ssp. major) natural populations exposed to different environmental conditions

In the present study, developmental stability of leaf traits was examined in three natural populations of Plantago major L. (ssp. major), representing two polluted environments (Karaburma and Zemun) and an unpolluted area (Crni Lug). Developmental stability was assessed as fluctuating asymmetry (FA). The magnitude of FA is believed to reflect differences in the ability of individuals to buffer their development in natural populations. We hypothesized that there are differences within characters and among characters in response to environmental conditions. Significant patterns of asymmetry correlations and asymmetry changes were detected both within characters and between characters. The manova results revealed a significant effect of individual and a significant individual × environment interaction on actual asymmetry (logL_i ? logR_i) and on the amount of asymmetry |(logL_i ? logR_i)| for leaf width and vein distances within a leaf. Over time, statistically significant and positive correlations of the FA values were detected for each trait separately per sample (population). For both leaf traits, there were differences for (logL_i ? logR_i) and |(logL_i ? logR_i)| asymmetry values among individuals within samples in response to yearly variations. Statistically significant and negative correlations for (logL_i ? logR_i) versus |(logL_i ? logR_i)| asymmetries were detected for both leaf traits. In summary, our results highlight the importance of differences in the ability of individuals to buffer their development under different environmental conditions and point to the concept that developmental stability is character specific.     

FLUCTUATING ASYMMETRY IN A SALIX HYBRID SYSTEM: THE IMPORTANCE OF GENETIC VERSUS ENVIRONMENTAL CAUSES

To examine the effects of hybridization and environmental stress on developmental instability, we examined fluctuating asymmetry (FA), the variance in random deviations from perfect symmetry in bilaterally symmetrical traits, for leaf symmetry in a Salix hybrid system. An abiotic environmental stress (water stress), an interspecific biotic stress (pathogen attack), and an intraspecific biotic stress (competition) were examined to determine which factors increase developmental instability. None of these three environmental stressors significantly increased FA. However, genetic stress through hybridization was detected; hybrid plants showed significantly higher levels of FA than parental species. In contrast to hybridization providing greater developmental stability through heterozygosity, these results suggest that complex, nonadditive interactions provided developmental stability and that developmental instability increased when coadapted gene complexes were disrupted through hybridization. In addition, plant biomass was significantly, negatively correlated with FA, suggesting that those individuals that were more able to buffer themselves against the disruptive effects of environmental stress may have a selective advantage over those that are less able to buffer themselves against these disruptive effects.     

EVOLUTION OF VARIATION AND VARIABILITY UNDER FLUCTUATING,STABILIZING, AND DISRUPTIVE SELECTION

How variation and variability (the capacity to vary) may respond to selection remain open questions. Indeed, effects of different selection regimes on variational properties, such as canalization and developmental stability are under debate. We analyzed the patterns of among‐ and within‐individual variation in two wing‐shape characters in populations of Drosophila melanogaster maintained under fluctuating, disruptive, and stabilizing selection for more than 20 generations. Patterns of variation in wing size, which was not a direct target of selection, were also analyzed. Disruptive selection dramatically increased phenotypic variation in the two shape characters, but left phenotypic variation in wing size unaltered. Fluctuating and stabilizing selection consistently decreased phenotypic variation in all traits. In contrast, within‐individual variation, measured by the level of fluctuating asymmetry, increased for all traits under all selection regimes. These results suggest that canalization and developmental stability are evolvable and presumably controlled by different underlying genetic mechanisms, but the evolutionary responses are not consistent with an adaptive response to selection on variation. Selection also affected patterns of directional asymmetry, although inconsistently across traits and treatments.     

A meta-analysis of the heritability of developmental stability

The existence of additive genetic variance in developmental stability has important implications for our understanding of morphological variation. The heritability of individual fluctuating asymmetry and other measures of developmental stability have frequently been estimated from parent-offspring regressions, sib analyses, or from selection experiments. Here we review by meta-analysis published estimates of the heritability of developmental stability, mainly the degree of individual fluctuating asymmetry in morphological characters. The overall mean effect size of heritabilities of individual fluctuating asymmetry was 0.19 from 34 studies of 17 species differing highly significantly from zero (P < 0.0001). The mean heritability for 14 species was 0.27. This indicates that there is a significant additive genetic component to developmental stability. Effect size was larger for selection experiments than for studies based on parent-offspring regression or sib analyses, implying that genetic estimates were unbiased by maternal or common environment effects. Additive genetic coefficients of variation for individual fluctuating asymmetry were considerably higher than those for character size per se. Developmental stability may be significantly heritable either because of strong directional selection, or fluctuating selection regimes which prevent populations from achieving a high degree of developmental stability to current environmental and genetic conditions.     

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

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

DEVELOPMENTAL INSTABILITY IN WILD CHROMOSOMAL HYBRIDS OF THE HOUSE MOUSE

In wild populations of the house mouse from Tunisia, fluctuating asymmetry and character size of tooth traits were compared between chromosomal races (2n = 40, all acrocentric standard karyotype, and 2n = 22, with nine fixed Robertsonian fusions) and their natural hybrids. Developmental stability was impaired in hybrids compared to both parental groups. Because genetic divergence measured by allozyme markers was low, genomic incompatibilities were not expected between the chromosomal races. This suggests that differentiation of gene systems specifically involved in development may have occurred between the chromosomal races. Support for the latter was found in the study of character size which showed that the 2n = 22 mice had smaller teeth than either the hybrid or the standard mice. The study of Tunisian chromosomal races thus shows that chromosomal evolution may lead to important changes in coadapted gene systems without involving extensive genic differentiation.     

ELECTROPHORETIC CONFIRMATION OF INTERSPECIFIC HYBRIDIZATION IN AESCULUS (HIPPOCASTANACEAE) AND THE GENETIC STRUCTURE OF A BROAD HYBRID ZONE

Within a broad (>200 km wide) hybrid zone involving three parapatric species of Aesculus, we observed coincident clines in allele frequency for 6 of 14 electrophoretic loci. The cooccurrence of alleles characteristic of A. pavia, A. sylvatica, and A. flava was used to estimate genetic admixtures in 48 populations involving various hybrids between these taxa in the southeastern United States. High levels of allelic polymorphism (up to 40% greater than the parental taxa) were observed in hybrid populations and also in some populations bordering the hybrid zone. A detailed analysis of a portion of the hybrid zone involving A. pavia and A. sylvatica revealed a highly asymmetrical pattern of gene flow, predominantly from Coastal Plain populations of A. pavia into Piedmont populations of A. sylvatica. Computer simulations were used to generate expected genotypic arrays for parental, F₁; and backcross individuals, which were compared with natural populations using a character index scoring system. In these comparisons, hybrid individuals could be distinguished from either parent, but F₁ and backcross progeny could not be distinguished from each other. Most hybrid populations were found to include hybrids and one of the parental taxa, but never both parents. Three populations appeared to be predominantly hybrids with no identifiable parental individuals. Hybrids occurred commonly at least 150 km beyond the range of A. pavia, but usually not more than 25 km beyond the range of A. sylvatica. Introgression, suggested by genetically hybrid individuals and significant gene admixtures of two or more species in populations lacking morphological evidence of hybridization, may extend the hybrid zone further in both directions. The absence of one or both parental species from hybrid populations implies a selective disadvantage to parentals in the hybrid zone and/or that hybridization has occurred through long-distance gene flow via pollen, primarily from A. pavia into A. sylvatica. Long-distance pollen movement in plants may generate hybrid zones of qualitatively different structure than those observed in animals, where gene flow involves dispersal of individuals.     

Developmental stability is not disrupted by extensive hybridization and introgression among populations of the marine bivalve molluscs Mytilus edulis (L.) and M. galloprovincialis (Lmk.) from south-west England

The effects of hybridization and introzgression were assessed among two naturally hybridizing bivalve molluscs (the mussels Mytilus edulis and M. galloprovincialis) from western Europe to estimate how disruptive these processes are to developmental stability (measured in terms of morphological variability). Ten shell traits were measured for 392 mussels from four allopatric populations (two each of At. edulis and At. galloprovincialis) and two hybrid populations. An index of variability (defined as Z_i= |y_i–y_i where y_; is the population mean of the length-standardized trait, and y_i is the individualcar;s length-standardized trait value) was constructed for each trait, and for the sum of the traits. The hybrid populations did not exhibit greater mean variability than the allopatric populations for any of the indices. Upon pooling, the hybrid populations had significantly lower variability than the pooled M. edulis populations and the pooled M. galloprovincialis populations in two analyses, and had similar means in the remaining nine analyses. Where significant differences existed, the pooled M. galloprovincialis had lower levels of mean trait variability than the pooled M. edulis. Among the two hybrid populations, the putative Fl hybrids and backcross individuals exhibited means of trait variability which were similar to those of the parental types. Thus, extensive hybridization and introgression do not adversely affect developmental stability among these mussel populations. There was a strong significant correlation between the ranking of indices (based on the amount of variability) across all six populations, indicating that a large genetic component determines the measured morphological variability. It is concluded that the genes or gene complexes which control morphological development in M. edulis and M. galloprovincialis arc very similar, providing further evidence of the close evolutionary relatedness of these mussel taxa.     

SEXUAL SELECTION,VIABILITY SELECTION,AND DEVELOPMENTAL STABILITY IN THE DOMESTIC FLY MUSCA DOMESTICA

Associations between developmental stability, sexual selection, and viability selection were studied in the domestic fly Musca domestica (Diptera, Muscidae). Developmental stability of the wings and tibia of flies of both sexes, measured in terms of their level of fluctuating asymmetry, was positively associated with mating success in free ranging populations and in sexual selection experiments. Mated individuals may have obtained indirect fitness benefits from sexual selection of two different kinds. First, the entomopathogenic fungus Enthomophthora muscae (Zygomycetes, Entomophthorales) infects and kills adult domestic flies, and flies dead from fungus infections had more asymmetric wings than flies dead for other reasons. Experimental deposition of fungus spores on uninfected flies demonstrated that flies with asymmetric wings were more susceptible to fungus infections than flies with symmetric wings. Second, domestic flies were frequently eaten by insectivorous barn swallows Hirundo rustica, and flies depredated by birds had more asymmetric wings and tibia than surviving flies.     

FLUCTUATING ASYMMETRY IN CENTRAL AND MARGINAL POPULATIONS OF LYCHNIS VISCARIA IN RELATION TO GENETIC AND ENVIRONMENTAL FACTORS

Developmental instability in the form of increased fluctuating asymmetry can be caused by either genetic or environmental stress. Because extinctions can be attributed broadly to these factors, fluctuating asymmetry may provide a sensitive tool for detecting such stresses. We studied the level of fluctuating asymmetry of flowers of a perennial outcrossing plant species, Lychnis viscaria, both in natural and common-garden populations. The degree of flower asymmetry was higher in small, isolated, and marginal populations of the species range. These marginal populations also were the most homozygous. In the core area of the species' range, flowers were more symmetrical The level of asymmetry was correlated with both population size and heterozygosity. However, a partial correlation analysis revealed that when the impact of population size was controlled for, there was a negative relationship between fluctuating asymmetry and heterozygosity, whereas when controlling for heterozygosity, no relationship between population size and fluctuating asymmetry was found. This indicates that genetic consequences of small population size probably underlie the relationship between the level of asymmetry and population size. Results from a transplantation experiment showed that individuals subjected to a higher environmental stress had an increased level of asymmetry compared to control plants. In the common-garden conditions the level of fluctuating asymmetry did not differ between the central and marginal populations. This suggests that presumably both genetic and environmental factors affected to the higher level of asymmetry among marginal populations compared to central ones. In all we conclude that even though fluctuating asymmetry seems to be a sensitive tool for detecting stresses, results from studies focusing on only one factor should be interpreted with caution.     

Fluctuating Asymmetry as an Indicator of Environmental Stress From Off-Highway Vehicles

Abstract: With human activities increasingly impacting natural resources in relatively remote locations, there is a need for simple and efficient methods to explore the ecological consequences of these activities. Little is understood about the influences of off-highway vehicle (OHV) use on wildlife populations. We examined the effect of OHV activity on developmental instability in a phrynosomatid lizard (i.e., western fence lizard [Sceloporus occidentalis]) in the western Great Basin, USA. We measured fluctuating asymmetry (FA) of bilateral head-scale patterns in populations of lizards at 3 OHV and 3 non-OHV sites. Fluctuating asymmetry was higher at OHV sites relative to non-OHV sites, supporting the idea that OHV activity can stress wildlife populations. We found FA to be a good tool for uncovering responses to stress in natural populations, and we recommend exploring FA as a means of uncovering developmental instability in other systems that merit conservation interest.     

Null alleles at two lactate dehydrogenase loci in rainbow trout are associated with decreased developmental stability

Previous studies with rainbow trout (Oncorhynchus mykiss) have shown that allozymic heterozygotes have increased developmental stability, as measured by reduced fluctuating bilateral asymmetry. In this paper, we examine the phenotypic effects of null alleles at two lactate dehydrogenase (LDH) loci. If the association between allozymic heterozygosity and developmental stability is due largely to linked chromosomal segments, then we would expect null allele heterozygotes to have increased developmental stability. In contrast, heterozygotes for LDH null alleles in three populations have reduced developmental stability. This suggests that the reduction in enzyme activity at these loci is having a deleterious effect on development that is strong enough to mask any beneficial effects that may be associated with heterozygosity for these chromosomal segments. The LDH loci examined in this study are members of two different paralogous pairs of duplicate genes produced by the polyploidization of the ancestral salmonid genome. The apparent deleterious effects of these null alleles in heterozygotes could retard the possible loss of duplicate gene expression.     

Use of a geometric morphometric method to determine the developmental stability of <Emphasis Type="Italic">Betula pendula</Emphasis> Roth

A geometric morphometric method has been proposed to test the fluctuating asymmetry and the developmental stability of Betula pendula Roth populations. The main factors affecting the developmental stability were the industrial emission level, the relief altitude, and the interaction of both these factors. A strong correlation between the fluctuating asymmetry indices obtained by the normalizing difference method and geometric morphometric method has been revealed. The fluctuating asymmetry determined by the geometric morphometric method is sensitive to the presence of directional asymmetry, which makes it possible to use this method for precise bioindication mapping of the developmental stability.     

Analysis of asymmetries in the African fruit bats Eidolon helvum and Rousettus egyptiacus (Mammalia: Megachiroptera) from the islands of the Gulf of Guinea. II. Integration and levels of multivariate fluctuating asymmetry across a geographical range

Using a set of cranial morphometric characters, trends of variation in multivariate fluctuating asymmetry were evaluated and compared in populations of African fruit bats Rousettus egyptiacus and Eidolon helvum from the Gulf of Guinea islands, and the adjacent mainland. Levels of asymmetry were compared across populations and species, and significant differences were found in both comparisons. Differences coincided with species‐specific patterns of morphological and genetic differentiation. Concordance of correlation matrices of asymmetry was also compared. Results were significant; concordance is hypothesized to be a by‐product of developmental processes that produce the ‘fox‐like’ morphology shared by these species. Consistency of asymmetry patterns suggests that the developmental pathway producing it is highly canalized. A prediction of the above hypothesis is that a radical change in the ‘fox‐like’ structural pattern would result in breakage of the asymmetry parameter associated with it.