Lack of response to artificial selection on developmental stability of partial wing shape components in Drosophila melanogaster

Developmental stability, the ability of organisms to buffer their developmental processes against developmental noise is often evaluated with fluctuating asymmetry (FA). Natural genetic variation in FA has been investigated using Drosophila wings as a model system and the recent estimation of the heritability of wing shape FA was as large as 20 %. Because natural genetic variation in wing shape FA was found to localize in a partial component of the wings, heritable variation in specific parts of the wings might be responsible for FA estimation based on the whole wing shape. In this study, we quantified the shape of three partial components of the wings, and estimated the heritability of the wing shape FA based on artificial selections. As a result, FA values for the partial wing shape components did not respond to artificial selections and the heritability scores estimated were very small. These results indicate that natural additive genetic variation in FA of partial wing components was very small compared with that in a complex wing trait.     

QUANTITATIVE GENETICS OF BRYOZOAN PHENOTYPIC EVOLUTION. III. PHENOTYPIC PLASTICITY AND THE MAINTENANCE OF GENETIC VARIATION

Cheilostome bryozoan species show long-term morphologic stasis, implying stabilizing selection sustained for millions of years, but nevertheless retain significant heritable variation in traits of skeletal morphology. The possible role of within-genotype (within-colony) phenotypic variability in preserving genetic diversity was analyzed using breeding data for two species of Stylopoma from sites along 110 km of the Caribbean coast of Panama. Variation among zooids within colonies accounts for nearly two-thirds of the phenotypic variance on average, increases with environmental heterogeneity, and includes significant genotype-environment interaction. Thus, within-colony variability apparently represents phenotypic plasticity, at least some of which is heritable, rather than random “developmental noise.” Almost all of the among-colonies component of phenotypic variance is accounted for by additive genetic differences in trait means, suggesting that within-colony plasticity includes virtually all of the environmental component of phenotypic variance in these populations of Stylopoma. Thus, heritable within-colony plasticity could play a significant part in maintaining genetic diversity in cheilostomes, but it is also possible that rates of polygenic mutation alone are sufficient to balance the effects of selection.     

Genetic mapping of developmental instability: design, model and algorithm

Developmental instability or noise, defined as the phenotypic imprecision of an organism in the face of internal or external stochastic disturbances, has been thought to play an important role in shaping evolutionary processes and patterns. The genetic studies of developmental instability have been based on fluctuating asymmetry (FA) that measures random differences between the left and the right sides of bilateral traits. In this article, we frame an experimental design characterized by a spatial autocorrelation structure for determining the genetic control of developmental instability for those traits that cannot be bilaterally measured. This design allows the residual environmental variance of a quantitative trait to be dissolved into two components due to permanent and random environmental factors. The degree of developmental instability is quantified by the relative proportion of the random residual variance to the total residual variance. We formulate a mixture model to estimate and test the genetic effects of quantitative trait loci (QTL) on the developmental instability of the trait. The genetic parameters including the QTL position, the QTL effects, and spatial autocorrelations are estimated by implementing the EM algorithm within the mixture model framework. Simulation studies were performed to investigate the statistical behavior of the model. A live example for poplar trees was used to map the QTL that control root length growth and its developmental instability from cuttings in water culture.     

The Developmental Instability—Sexual Selection Hypothesis: A General Evaluation and Case Study

Developmental instability results from small, random perturbations to developmental processes of individual traits. Phenotypic outcomes of developmental instability include fluctuating asymmetry (FA, subtle deviations from perfect bilateral symmetry) and phenodeviance (minor morphological abnormalities). A great deal of research over the past 18 years has focused on the role of developmental instability in sexual selection. A driving force behind this research has been the developmental instability-sexual selection hypothesis, which posits that symmetry and lack of phenodeviance in secondary sexual traits are assessed by mates and rivals because they provide a reliable cue of individual genetic quality. The present article tests this hypothesis by evaluating its five main predictions using published results: expressions of developmental instability in secondary sexual traits should be (1) negatively correlated with mating success; (2) directly assessed by mates and sexual rivals; (3) heritable; (4) condition-dependent; and (5) negatively correlated with ornament size. The first two predictions receive considerable, though not ubiquitous, support from a range of animal species. However, FA in secondary sexual traits is generally not significantly heritable, indicating that FA is unlikely to reveal genetic quality that can be transmitted to offspring. Similarly, there is little evidence to support the predictions that FA is condition dependent, and that it is negatively phenotypically or genetically correlated with sexual trait size. Based on an evaluation of the evidence overall, it is concluded that this hypothesis is unlikely to be viable; it appears unlikely that mate choice for symmetry evolves by “good genes” sexual selection. Hypotheses that do not require asymmetry and phenodeviance to reveal heritable genetic quality may explain observed links between FA/phenodeviance and mating success. Results of a case study of Drosophila bipectinata are summarized, which reinforce this general conclusion. It is suggested that nonadditive genetic variation arising from an interaction between trait-specific developmental genes and genetic background may drive sexual selection for reducing developmental instability in some cases. Levels of developmental instability variation in a population may need to surpass a critical threshold for sexual selection to operate, possibly explaining some of the pronounced heterogeneity in the effect of developmental instability on sexual selection reported in the literature.     

PLASTICITY, CANALIZATION, AND DEVELOPMENTAL STABILITY OF THE DROSOPHILA WING: JOINT EFFECTS OF MUTATIONS AND DEVELOPMENTAL TEMPERATURE

The phenotypic effects of genetic and environmental manipulations have been rarely investigated simultaneously. In addition to phenotypic plasticity, their effect on the amount and directions of genetic and phenotypic variation is of particular evolutionary importance because these constitute the material for natural selection. Here, we used heterozygous insertional mutations of 16 genes involved in the formation of the Drosophila wing. The flies were raised at two developmental temperatures (18°C and 28°C). Landmark-based geometric morphometrics was used to analyze the variation of the wing size and shape at different hierarchical levels: among genotypes and temperatures; among individuals within group; and fluctuating asymmetry (FA). Our results show that (1) the phenotypic effects of the mutations depend on temperature; (2) reciprocally, most mutations affect wing plasticity; (3) both temperature and mutations modify the levels of FA and of among individuals variation within lines. Remarkably, the patterns of shape FA seem unaffected by temperature whereas those associated with individual variation are systematically altered. By modifying the direction of available phenotypic variation, temperature might thus directly affect the potential for further evolution. It suggests as well that the developmental processes responsible for developmental stability and environmental canalization might be partially distinct.     

A QUANTITATIVE-GENETIC MODEL FOR SELECTION ON DEVELOPMENTAL NOISE

We propose a simple model for analyzing the effects of microenvironmental variation in quantitative genetics. Our model assumes that the sensitivity of the phenotype to fluctuations in microenvironment has a genetic basis and allows for genetic correlation between trait value and microenvironmental sensitivity. We analyze the effects of short-term stabilizing and directional selection on the genotypic and microenvironmental components of phenotypic variance. Our model predicts that stabilizing selection on a quantitative trait increases developmental canalization. We show that stabilizing selection can result in an increase in the heritability. Our findings may provide an explanation for the results of selection experiments in which artificial stabilizing selection did not change the heritability coefficient or increased it.     

THE ASSOCIATION BETWEEN FLUCTUATING ASYMMETRY,TRAIT VARIABILITY,TRAIT HERITABILITY,AND STRESS: A MULTIPLY REPLICATED EXPERIMENT ON COMBINED STRESSES IN DROSOPHILA MELANOGASTER

A number of hypotheses have been proposed about the association between developmental stability phenotypic variability, heritability, and environmental stress. Stress is often considered to increase both the asymmetry and phenotypic variability of bilateral traits, although this may depend on trait heritability. Empirical studies of such associations often yield inconsistent results. This may reflect the diversity of traits and conditions used or a low repeatability of any associations. To test for repeatable associations between these variables, multiply replicated experiments were undertaken on Drosophila melanogaster using a combination stress at the egg, larval and adult stages of reduced protein, ethanol in the medium, and a cold shock. Both metric and meristic traits were measured and levels of heritable variation for each trait estimated by maximum likelihood and parent-offspring regression over three generations. Trait means were reduced by stress, whereas among-individual variation increased Fluctuating asymmetry (FA) was increased by stress in some cases, but few comparisons were significant. Only one trait orbital bristle, showed consistent increases in FA. Changes in trait means, trait phenotypic variability, and developmental stability as a result of stress were not correlated. Extreme phenotypes tended to have higher levels of FA but only the results for orbital bristles were significant. All traits had low to intermediate heritabilities except orbital bristle, which showed no heritable variation. Only traits with low heritability and high levels of phenotypic variability may show consistent increases in FA under stress. Overall, the independence of phenotypic variability, plasticity, and the developmental stability of traits extend to changes in these measures under stressful conditions.     

Artificial selection reveals heritable variation for developmental instability

Fluctuating (nondirectional) asymmetry (FA) of bilaterally paired structures on a symmetrical organism is commonly used to assay the developmental instability (DI) caused by environmental or genetic factors. Although evidence for natural selection to reduce FA has been reported, evidence that FA (and by extension DI) is heritable is weak. We report the use of artificial selection to demonstrate heritable variation in the fluctuating asymmetry of interlandmark distances within the wing in an outbred population of Drosophila melanogaster. Our estimates for the heritability of FA range from 0% to 1% and result in estimates for the heritability of DI as large as 20%, comparable to values typical for life-history traits. These values indicate the existence of evolutionarily relevant genetic variation for DI and the effectiveness of selection for reduced FA suggests that natural selection has not fixed all the genetic variants that would improve developmental stability in these populations.     

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.     

Temperature and genotypic effects on life history and fluctuating asymmetry in a field strain of Culex pipiens

Fluctuating asymmetry (FA) has been proposed as a tool to measure levels of stress experienced by populations of organisms during development. To be of value as a bio-marker to highlight conditions at particular sites, it is important that variation in FA is due to environmental (eg pollution) variation and not genetic variation among populations and families, in other words heritability for FA should be very close to zero. A full-sib design was set up in which families of Culex pipiens mosquitoes collected from the field were reared at three different developmental temperatures. The effects of temperature and family on developmental rate, egg to adult survival and four wing morphological measures were assessed. There was both a temperature and a family effect on development rate and survival. Temperature affected all four wing traits, but an influence of family was only evident in two of the wing traits. Two separate measures of FA for each of the wing traits were obtained. The mean estimates of FA were mainly around 1% of the value of the character measured. There was evidence of an increase in FA with increase in temperature stress. Heritability was estimated for the wing traits and wing trait FA's using restricted estimation maximum likelihood. The estimates of heritability for the wing traits were small and, individually, did not differ significantly from zero. There was also no evidence of heritable genetic variation for any of the wing trait FA's. The results are discussed in relation to other studies where FA heritabilities have been estimated and in relation to the use of FA as an indicator of environmental stress.     

Epigenetic population differentiation in field‐ and common garden‐grown Scabiosa columbaria plants

Populations often differ in phenotype and these differences can be caused by adaptation by natural selection, random neutral processes, and environmental responses. The most straightforward way to divide mechanisms that influence phenotypic variation is heritable variation and environmental‐induced variation (e.g., plasticity). While genetic variation is responsible for most heritable phenotypic variation, part of this is also caused by nongenetic inheritance. Epigenetic processes may be one of the underlying mechanisms of plasticity and nongenetic inheritance and can therefore possibly contribute to heritable differences through drift and selection. Epigenetic variation may be influenced directly by the environment, and part of this variation can be transmitted to next generations. Field screenings combined with common garden experiments will add valuable insights into epigenetic differentiation, epigenetic memory and can help to reveal part of the relative importance of epigenetics in explaining trait variation. We explored both genetic and epigenetic diversity, structure and differentiation in the field and a common garden for five British and five French Scabiosa columbaria populations. Genetic and epigenetic variation was subsequently correlated with trait variation. Populations showed significant epigenetic differentiation between populations and countries in the field, but also when grown in a common garden. By comparing the epigenetic variation between field and common garden‐grown plants, we showed that a considerable part of the epigenetic memory differed from the field‐grown plants and was presumably environmentally induced. The memory component can consist of heritable variation in methylation that is not sensitive to environments and possibly genetically based, or environmentally induced variation that is heritable, or a combination of both. Additionally, random epimutations might be responsible for some differences as well. By comparing epigenetic variation in both the field and common environment, our study provides useful insight into the environmental and genetic components of epigenetic variation.     

Natural genetic variation in fluctuating asymmetry of wing shape in Drosophila melanogaster

Fluctuating asymmetry (FA), defined as random deviation from perfect symmetry, has been used to assay the inability of individuals to buffer their developmental processes from environmental perturbations (i.e., developmental instability). In this study, we aimed to characterize the natural genetic variation in FA of wing shape in Drosophila melanogaster, collected from across the Japanese archipelago. We quantified wing shapes at whole wing and partial wing component levels and evaluated their mean and FA. We also estimated the heritability of the mean and FA of these traits. We found significant natural genetic variation in all the mean wing traits and in FA of one of the partial wing components. Heritability estimates for mean wing shapes were significant in two and four out of five wing traits in males and females, respectively. On the contrary, heritability estimates for FA were low and not significant. This is a novel study of natural genetic variation in FA of wing shape. Our findings suggest that partial wing components behave as distinct units of selection for FA, and local adaptation of the mechanisms to stabilize developmental processes occur in nature.     

THE EVOLUTION OF PHENOTYPIC CORRELATIONS AND “DEVELOPMENTAL MEMORY”

Development introduces structured correlations among traits that may constrain or bias the distribution of phenotypes produced. Moreover, when suitable heritable variation exists, natural selection may alter such constraints and correlations, affecting the phenotypic variation available to subsequent selection. However, exactly how the distribution of phenotypes produced by complex developmental systems can be shaped by past selective environments is poorly understood. Here we investigate the evolution of a network of recurrent nonlinear ontogenetic interactions, such as a gene regulation network, in various selective scenarios. We find that evolved networks of this type can exhibit several phenomena that are familiar in cognitive learning systems. These include formation of a distributed associative memory that can “store” and “recall” multiple phenotypes that have been selected in the past, recreate complete adult phenotypic patterns accurately from partial or corrupted embryonic phenotypes, and “generalize” (by exploiting evolved developmental modules) to produce new combinations of phenotypic features. We show that these surprising behaviors follow from an equivalence between the action of natural selection on phenotypic correlations and associative learning, well‐understood in the context of neural networks. This helps to explain how development facilitates the evolution of high‐fitness phenotypes and how this ability changes over evolutionary time.     

Developmental stability in yellow dung flies (Scathophaga stercoraria): fluctuating asymmetry,heterozygosity and environmental stress

The genetic basis for developmental stability, the ability of an organism to withstand genetic and environmental disturbance of development, is poorly understood. Fluctuating asymmetry (FA: small random deviations from symmetry in paired, bilateral traits) is the most widely used measure of developmental stability, and evidence suggests FA is weakly and negatively associated with genome‐wide heterozygosity. We investigated the genetic basis of developmental stability in the yellow dung fly. Fly lines were inbred for 16 generations at which time they were homozygous at the phosphoglucomutase (PGM) loci and PGM appears to influence FA in at least one other taxon. After 16 generations of inbreeding, lines homozygous for different PGM alleles were crossed and levels of FA for four metric traits were compared in the inbred and crossed flies. We also compared FA levels in these flies with previously gathered data on wild‐type (second generation outcrossed) flies, and additionally looked at the effects of two environmental stresses (larval food limitation and increased temperature) on FA. There were no significant differences in any measure of FA, nor in mean FA, in any trait when inbred and crossed flies were compared. Comparison of FA in these and wild flies also revealed no significant differences. Food limitation had no influence on FA, whereas heat stress increased FA of naturally, but not sexually, selected traits. Our results do not show a negative relationship between heterozygosity and FA, but support the notion that FA levels are stress, trait and taxon specific.     

Deficiency mapping of the genomic regions associated with effects on developmental stability in Drosophila melanogaster

Developmental stability is the tendency of morphological traits to resist the effects of developmental noise, and is commonly evaluated by examining fluctuating asymmetry (FA)-random deviations from perfect bilateral symmetry. Molecular mechanisms that control FA have been a long-standing topic of debate in the field of evolutionary biology and quantitative genetics. In this study, we mapped genomic regions associated with effects on the mean and FA of morphological traits, and characterized the trait specificity of those regions. A collection of isogenic deficiency strains established by the DrosDel project was used for deficiency mapping of genome regions associated with effects on FA. We screened 435 genome deficiencies or approximately 64.9% of the entire genome of Drosophila melanogaster to map the region that demonstrated a significant effect on FA of morphological traits. We found that 406 deficiencies significantly affected the mean of morphological traits, and 92 deficiencies increased FA. These results suggest that several genomic regions have the potential to affect developmental stability. They also suggest the possibility of the existence of trait-specific and trait-nonspecific mechanisms for stabilizing developmental processes. The new findings in this study could provide insight into the understanding of the genetic architecture underlying developmental stability.     

A general definition of the heritable variation that determines the potential of a population to respond to selection

Genetic selection is a major force shaping life on earth. In classical genetic theory, response to selection is the product of the strength of selection and the additive genetic variance in a trait. The additive genetic variance reflects a population's intrinsic potential to respond to selection. The ordinary additive genetic variance, however, ignores the social organization of life. With social interactions among individuals, individual trait values may depend on genes in others, a phenomenon known as indirect genetic effects. Models accounting for indirect genetic effects, however, lack a general definition of heritable variation. Here I propose a general definition of the heritable variation that determines the potential of a population to respond to selection. This generalizes the concept of heritable variance to any inheritance model and level of organization. The result shows that heritable variance determining potential response to selection is the variance among individuals in the heritable quantity that determines the population mean trait value, rather than the usual additive genetic component of phenotypic variance. It follows, therefore, that heritable variance may exceed phenotypic variance among individuals, which is impossible in classical theory. This work also provides a measure of the utilization of heritable variation for response to selection and integrates two well-known models of maternal genetic effects. The result shows that relatedness between the focal individual and the individuals affecting its fitness is a key determinant of the utilization of heritable variance for response to selection.     

Heritability of asymmetry and lateral plate number in the threespine stickleback

The estimation of individual fitness and quality are important elements of evolutionary ecological research. Over the past six decades, there has been great interest in using fluctuating asymmetry (FA) to represent individual quality, yet, serious technical problems have hampered efforts to estimate the heritability of FA, which, in turn, has limited progress in the investigation of FA from an evolutionary perspective. Here we estimate the heritability of number of lateral plates, their FA and directional asymmetry (DA) in threespine stickleback, Gasterosteus aculeatus. By (i) using a meristic trait and (ii) basing our calculations on a large half-sib design experiment involving 2,079 offspring from 84 families, we overcame many of the difficulties faced by earlier FA studies. Both lateral plate number and FA in lateral plates were heritable (h² = 0.46 and 0.21, respectively), even after controlling for marker genotypes linked to EDA (the major locus influencing plate number). Likewise, DA in lateral plates was heritable h² = 0.23). The additive genetic component of FA in lateral plates makes it a prime candidate for further investigation into the evolutionary implications of FA and the genetic underpinnings of developmental instability. This discovery in an evolutionary model species holds the possibility to invigorate the study of FA from an evolutionary perspective.     

A Novel Statistical Model to Estimate Host Genetic Effects Affecting Disease Transmission

There is increasing recognition that genetic diversity can affect the spread of diseases, potentially affecting plant and livestock disease control as well as the emergence of human disease outbreaks. Nevertheless, even though computational tools can guide the control of infectious diseases, few epidemiological models can simultaneously accommodate the inherent individual heterogeneity in multiple infectious disease traits influencing disease transmission, such as the frequently modeled propensity to become infected and infectivity, which describes the host ability to transmit the infection to susceptible individuals. Furthermore, current quantitative genetic models fail to fully capture the heritable variation in host infectivity, mainly because they cannot accommodate the nonlinear infection dynamics underlying epidemiological data. We present in this article a novel statistical model and an inference method to estimate genetic parameters associated with both host susceptibility and infectivity. Our methodology combines quantitative genetic models of social interactions with stochastic processes to model the random, nonlinear, and dynamic nature of infections and uses adaptive Bayesian computational techniques to estimate the model parameters. Results using simulated epidemic data show that our model can accurately estimate heritabilities and genetic risks not only of susceptibility but also of infectivity, therefore exploring a trait whose heritable variation is currently ignored in disease genetics and can greatly influence the spread of infectious diseases. Our proposed methodology offers potential impacts in areas such as livestock disease control through selective breeding and also in predicting and controlling the emergence of disease outbreaks in human populations.     

DEVELOPMENTAL QUANTITATIVE GENETICS AND THE EVOLUTION OF ONTOGENIES

A model is presented which permits integration of developmental information into genetic discussions about evolutionary change in morphology. Development of a trait is described in terms of an ontogenetic trajectory whose properties are defined by a small number of parameters. Some evolutionary aspects of development are examined from the perspective of this quantitative genetic model. Particular attention is given to the developmental origin of pleiotropic effects, developmental constraints, heterochrony, and the growth and morphogenesis of complex morphologies. The role of genetic maternal effects in mammalian development is briefly examined, particularly as it relates to selection on developmental traits.     

ONTOGENETIC VARIATION IN PATTERNS OF DEVELOPMENTAL AND FUNCTIONAL INTEGRATION IN SKULLS OF SIGMODON FULVIVENTER

Patterns of variation and covariation within populations can influence how characters respond to natural selection and random genetic drift and so constrain the ability of natural selection to modify the phenotype. We examined several potential developmental and functional explanations of character covariation throughout ontogeny using known-age samples of the cotton rat (Sigmodon fulviventer) to identify the causes of covariation and to assess the variability of patterns of covariation throughout postnatal growth. Competing developmental and functional models were fit to samples of orofacial and neurocranial measures by confirmatory factor analysis and evaluated for their ability to reconstruct observed variance-covariance matrices. Samples of successive ages were simultaneously fit to a common model to test the hypothesis that the patterns of developmental and functional integration were invariant between ages. Orofacial characters derived from the same branchial-arch primordium covary early in ontogeny. Subsequently, there is a repatterning of integration that may reflect a transition from developmental to functional sources of integration. Neurocranial characters exhibit even more variation in patterns of covariation: initially, characters appear to comprise a single integrated unit; before puberty, they appear to respond to localized bone growth; after puberty, they form separate calvarial and basicranial components. This ontogenetic variation in patterns of covariation suggests that developmental constraints are transient and flexible and that the consequences of selection may depend upon the age at which it acts.