Developmental interactions and the constituents of quantitative variation

Development is the process by which genotypes are transformed into phenotypes. Consequently, development determines the relationship between allelic and phenotypic variation in a population and, therefore, the patterns of quantitative genetic variation and covariation of traits. Understanding the developmental basis of quantitative traits may lead to insights into the origin and evolution of quantitative genetic variation, the evolutionary fate of populations, and, more generally, the relationship between development and evolution. Herein, we assume a hierarchical, modular structure of trait development and consider how epigenetic interactions among modules during ontogeny affect patterns of phenotypic and genetic variation. We explore two developmental models, one in which the epigenetic interactions between modules result in additive effects on character expression and a second model in which these epigenetic interactions produce nonadditive effects. Using a phenotype landscape approach, we show how changes in the developmental processes underlying phenotypic expression can alter the magnitude and pattern of quantitative genetic variation. Additive epigenetic effects influence genetic variances and covariances, but allow trait means to evolve independently of the genetic variances and covariances, so that phenotypic evolution can proceed without changing the genetic covariance structure that determines future evolutionary response. Nonadditive epigenetic effects, however, can lead to evolution of genetic variances and covariances as the mean phenotype evolves. Our model suggests that an understanding of multivariate evolution can be considerably enriched by knowledge of the mechanistic basis of character development.     

Evolution of pleiotropy: epistatic interaction pattern supports a mechanistic model underlying variation in genotype-phenotype map

The genotype-phenotype (GP) map consists of developmental and physiological mechanisms mapping genetic onto phenotypic variation. It determines the distribution of heritable phenotypic variance on which selection can act. Comparative studies of morphology as well as of gene regulatory networks show that the GP map itself evolves, yet little is known about the actual evolutionary mechanisms involved. The study of such mechanisms requires exploring the variation in GP maps at the population level, which presently is easier to quantify by statistical genetic methods rather than by regulatory network structures. We focus on the evolution of pleiotropy, a major structural aspect of the GP map. Pleiotropic genes affect multiple traits and underlie genetic covariance between traits, often causing evolutionary constraints. Previous quantitative genetic studies have demonstrated population-level variation in pleiotropy in the form of loci, at which genotypes differ in the genetic covariation between traits. This variation can potentially fuel evolution of the GP map under selection and/or drift. Here, we propose a developmental mechanism underlying population genetic variation in covariance and test its predictions. Specifically, the mechanism predicts that the loci identified as responsible for genetic variation in pleiotropy are involved in trait-specific epistatic interactions. We test this prediction for loci affecting allometric relationships between traits in an advanced intercross between inbred mouse strains. The results consistently support the prediction. We further find a high degree of sign epistasis in these interactions, which we interpret as an indication of adaptive gene complexes within the diverged parental lines.     

How to become large quickly: quantitative genetics of growth and foraging in a flush feeding lepidopteran larva

Rapid larval growth in insects may be selected for by rapid ephemeral phenological changes in food resources modifying the structure of phenotypic and genetic (co)variation in and among individual traits. We studied the relative effects of three processes which can modify expression of additive genetic and nongenetic variation in traits. First, natural selection tends to erode genetic variation in fitness-related traits. Second, there may be high variance even in traits closely coupled with fitness, if these traits are themselves products of variable lower level traits. Third, traits may be canalized by developmental processes which reduce phenotypic variation. Moreover, we investigated the phenotypic and genetic role played by the underlying traits in attaining simultaneously both large size and short development time. We measured phenotypic and genetic (co)variation in several pre- and post-ingestive foraging traits, growth, development rate, development time and size, together forming a hierarchical network of traits, in the larvae of a flush feeding geometrid, Epirrita autumnata. Rapid larval growth rate and high pupal mass are closely related to fitness in E. autumnata. Traits closely associated with larval growth displayed low levels of additive genetic variation, indicating that genetic variability may have been exhausted by selection for rapid growth. The body size of E. autumnata, in spite of its close correlation with fitness, exhibited a significant additive genetic variation, possiblye because caterpillar size is the outcome of many underlying heritable traits. The low level traits in the hierarchical net, number (indicating larval movements) and size of feeding bouts in leaves, relative consumption rate and efficiency of conversion of ingested food, displayed high levels of residual variation. High residual variation in consumption and physiological ability to handle leaf material resulted from their flexibility which reduced variation in growth rate, i.e. growth rate was canalized. We did not detect a trade-off between development time and final size. On the contrary, large pupal masses were attained by short larval periods, and this relationship was strongly genetically determined, suggesting that both developmental time and final size are expressions of the same developmental process (vigorous growth) and the same genes (or linkage disequilibrium).     

Phenotypic plasticity for life history traits in Drosophila melanogaster. II. Epigenetic mechanisms and the scaling of variances

Abstract We manipulated developmental time and dry weight at eclosion in 15 genotypes of Drosophila melanogaster by growing the larvae in 9 environments defined by 3 yeast concentrations at 3 temperatures. We observed how the genetic and various environmental components of phenotypic variation scaled with the mean values of the traits. Temperature, yeast, within-environmental factors and genotype influenced the genotypic and environmental standard deviations of the two traits in patterns that point to very different modes of physiological and developmental action of these factors. Since different factors affected the environmental and genetic components of the phenotypic variation either in parallel or inversely, we conclude that environmental heterogeneity may have small or large effects on evolutionary rates depending on which factors cause the heterogeneity. The analysis also suggests that the scaling of variances with the mean is not as trivial as is often assumed when coefficients of variation are computed to “standardize” variation.     

Founder effects and phenotypic variation in Adelges cooleyi, an insect pest introduced to the eastern United States

Introduced organisms experience founder effects including genetic bottlenecks that result in significant reductions in genetic variation. Genetic bottlenecks may constrain the evolution of phenotypic traits that facilitate success in novel habitats. We examined the effect of introduction into novel environments on genetic diversity of an insect pest, Adelges cooleyi, which was introduced into the eastern United States during the mid nineteenth century. We compared variation in mitochondrial and nuclear genomes in native and introduced samples to determine the effect of introduction on genetic variation experienced by this insect. We also measured an ecologically important phenotype, variation in host preference, in both native and introduced samples to compare variation in that trait with molecular genetic variation. To further investigate the relationship between genetic and phenotypic variation, we examined the degree to which mtDNA haplotypes provide information about host preference. Adelges cooleyi in eastern North America has significantly reduced genetic and phenotypic variation, but this low variation does not appear to have prevented persistence in a novel environment. Introduced insects appear to have retained host preference phenotypes similar to those of insects found where introductions likely originated.     

Effect of three types of ecological stress on the variability of morphological traits in Drosophila melanogaster

The effect of temperature, nutrition, and density stresses on phenotypic and genetic variation in morphological traits (thorax length, wing length, number of sternopleural and abdominal bristles, and number of arista branches) was examined in Drosophila melanogaster. In addition, the effect of stress on developmental stability measured as fluctuation asymmetry of bilateral traits was analyzed. All of the stresses were shown to increase phenotypic variation and fluctuating asymmetry of bilateral traits. Genetic variation of morphometric traits estimated using the isofemale line technique was higher under stressful than under normal conditions. Biotic and abiotic stresses were similar in their effect on phenotypic and genetic variation. The effect of stress on variability of morphometric traits was generally higher than on that of meristic traits. Possible causes of the increase of genetic variation under stress are discussed.     

Interpreting phenotypic variation in plants

Plant ecologists and evolutionary biologists frequently examine patterns of phenotypic variation across variable environments or genetic identities. Too often, we ignore the fact that most phenotypic traits change throughout growth and development of individual plants, and that rates of growth and development are highly variable. Plants growing in different environments are likely to grow at different rates, and will be of different sizes and stages of development at a particular age. When we compare plants as a function of plant size or developmental stage, as well as a function of age, we broaden our understanding of phenotypic variation between plants.     

Genotypic and phenotypic variation in transmission traits of a complex life cycle parasite

Characterizing genetic variation in parasite transmission traits and its contribution to parasite vigor is essential for understanding the evolution of parasite life‐history traits. We measured genetic variation in output, activity, survival, and infection success of clonal transmission stages (cercaria larvae) of a complex life cycle parasite (Diplostomum pseudospathaceum). We further tested if variation in host nutritional stage had an effect on these traits by keeping hosts on limited or ad libitum diet. The traits we measured were highly variable among parasite genotypes indicating significant genetic variation in these life‐history traits. Traits were also phenotypically variable, for example, there was significant variation in the measured traits over time within each genotype. However, host nutritional stage had no effect on the parasite traits suggesting that a short‐term reduction in host resources was not limiting the cercarial output or performance. Overall, these results suggest significant interclonal and phenotypic variation in parasite transmission traits that are not affected by host nutritional status.     

Contrasting levels of genotype by environment interaction for life history and morphological traits in invasive populations of Zaprionus indianus (Diptera: Drosophilidae)

It has been demonstrated that phenotypic plasticity and genotype by environment interaction are important for coping with new and heterogeneous environments during invasions. Zaprionus indianus Gupta (Diptera: Drosophilidae) is an Afrotropical invasive fly species introduced to the South American continent in 1999. This species is generalist and polyphagous, since it develops and feeds in several different fruit species. These characteristics of Z. indianus suggest that phenotypic plasticity and genotype by environment interaction may be important in this species invasion process. In this sense, our aim was to investigate the role of genetic variation for phenotypic plasticity (genotype by environment interaction) in Z. indianus invasion of the South American continent. Specifically, we quantified quantitative genetic variation and genotype by environment interactions of morphological and life history traits in different developmental environments, that is, host fruits. This was done in different populations in the invasive range of Z. indianus in Argentina. Results showed that Z. indianus populations have considerable amounts of quantitative genetic variation. Also, genotype by environment interactions was detected for the different traits analyzed in response to the different developmental environments. Interestingly, the amounts and patterns of these parameters differed between populations. We interpreted these results as the existence of differences in evolutionary potential between populations that have an important role in the short‐ and long‐term success of the Z. indianus invasion process.     

Phenotypic plasticity and genetic isolation-by-distance in the freshwater mussel <Emphasis Type="Italic">Unio pictorum</Emphasis> (Mollusca: Unionoida)

Freshwater mussels (Unionoida) show high intraspecific morphological variability, and some shell morphological traits are believed to be associated with habitat conditions. It is not known whether and which of these ecophenotypic differences reflect underlying genetic differentiation or are the result of phenotypic plasticity. Using 103 amplified fragment length polymorphism (AFLP) markers, we studied population genetics of three paired Unio pictorum populations sampled from two different habitat types (marina and river) along the River Thames. We found genetic differences along the Thames which were consistent with a pattern of isolation by distance and probably reflect limited dispersal via host fish species upon which unionoid larvae are obligate parasites. No consistent genetic differences were found between the two different habitat types suggesting that morphological differences in the degree of shell elongation and the shape of dorso-posterior margin are caused by phenotypic plasticity. Our study provides the first good evidence for phenotypic plasticity of shell shape in a European unionoid and illustrates the need to include genetic data in order properly to interpret geographic patterns of morphological variation.     

Genetic variation in response to an indirect ecological effect

Indirect ecological effects (IEEs) are widespread and often as strong as the phenotypic effects arising from direct interactions in natural communities. Indirect effects can influence competitive interactions, and are thought to be important selective forces. However, the extent that selection arising from IEEs results in long-term evolutionary change depends on genetic variation underlying the phenotypic response-that is, a genotype-by-IEE interaction. We provide the first data on genetic variation in the response of traits to an IEE, and illustrate how such genetic variation might be detected and analysed. We used a model tri-trophic system to investigate the effect of host plants on two populations of predatory ladybirds through a clonal aphid herbivore. A split-family experimental design allowed us to estimate the effects of aphid host plant on ladybird traits (IEE) and the extent of genetic variation in ladybird predators for response to these effects (genotype-by-indirect environmental effect interaction). We found significant genetic variation in the response of ladybird phenotypes to the indirect effect of host plant of their aphid prey, demonstrating the potential for evolutionary responses to selection arising from the prey host.     

Reduce, reuse, and recycle: developmental evolution of trait diversification

A major focus of evolutionary developmental (evo-devo) studies is to determine the genetic basis of variation in organismal form and function, both of which are fundamental to biological diversification. Pioneering work on metazoan and flowering plant systems has revealed conserved sets of genes that underlie the bauplan of organisms derived from a common ancestor. However, the extent to which variation in the developmental genetic toolkit mirrors variation at the phenotypic level is an active area of research. Here we explore evidence from the angiosperm evo-devo literature supporting the frugal use of genes and genetic pathways in the evolution of developmental patterning. In particular, these examples highlight the importance of genetic pleiotropy in different developmental modules, thus reducing the number of genes required in growth and development, and the reuse of particular genes in the parallel evolution of ecologically important traits.     

Genetic variation in larval period and pupal mass in an aphidophagous ladybird beetle (Harmonia axyridis) reared in different environments

Abstract Genetic trade‐offs for host plant use are hypothesized to facilitate the diversification of insect populations through specialization to their host plants. Previous studies mainly estimated the architecture of genetic variances and covariances in herbivorous species with discrete and limited types of host species. In contrast to herbivores, the relative abundance of resources for predatory species fluctuates in time and space, causing a more unpredictable encounter with prey species. The ecological characteristics of resource use might result in a differential mode of selection for herbivorous and predatory species, which could be reflected in a differential genetic architecture of developmental traits such as the duration of larval stage (henceforth referred to as larval period) and size of pupa (measured as pupal weight). This paper presents results from a study on the genetic architecture of larval period and pupal mass of an aphidophagous ladybird beetle, Harmonia axyridis Pallas, in different resource environments. Beetles reared on Acyrthosiphon pisum (Harris) showed a shorter developmental period and a heavier pupal mass than their siblings on Aphis craccivora Koch or on artificial diet, while the average larval period and pupal mass on A. craccivora and the artificial diet were similar. Further analyses of the genetic architecture suggest that the developmental traits on the two aphid species are genetically correlated, while there are only weak or no genetic correlations between these two traits on the two aphid preys and the artificial diet. Thus, the results suggest that the patterns of genotypic relationships between developmental traits differ from the phenotypic ones. The effects of past selection on the genetic architecture and the possible cause of the genetic correlation are discussed, as well as consequences for mass rearing for biological control.     

Plastic flies

Individuals within species and populations vary. Such variation arises through environmental and genetic factors and ensures that no two individuals are identical. However, it is clear that not all traits show the same degree of intraspecific variation. Some traits, in particular secondary sexual characteristics used by males to compete for and attract females, are extremely variable among individuals in a population. Other traits, for example brain size in mammals, are not. Recent research has begun to explore the possibility that the extent of phenotypic variation (here referred to as “variability”) may be a character itself and subject to natural selection. While these studies support the concept of variability as an evolvable trait, controversy remains over what precisely the trait is. At the heart of this controversy is the fact that there are very few examples of developmental mechanisms that regulate trait variability in response to any source of variation, be it environmental or genetic. Here, we describe a recent study from our laboratory that identifies such a mechanism. We then place the study in the context of current research on the regulation of trait variability, and discuss the implications for our understanding of the developmental regulation and evolution of phenotypic variation.     

Patterns of phenotypic covariation and correlation in modern humans as viewed from morphological integration

Proportionality of phenotypic and genetic distance is of crucial importance to adequately focus on population history and structure, and it depends on the proportionality of genetic and phenotypic covariance. Constancy of phenotypic covariances is unlikely without constancy of genetic covariation if the latter is a substantial component of the former. If phenotypic patterns are found to be relatively stable, the most probable explanation is that genetic covariance matrices are also stable. Factors like morphological integration account for such stability. Morphological integration can be studied by analyzing the relationships among morphological traits. We present here a comparison of phenotypic correlation and covariance structure among worldwide human populations. Correlation and covariance matrices between 47 cranial traits were obtained for 28 populations, and compared with design matrices representing functional and developmental constraints. Among-population differences in patterns of correlation and covariation were tested for association with matrices of genetic distances (obtained after an examination of 10 Alu-insertions) and with Mahalanobis distances (computed after craniometrical traits). All matrix correlations were estimated by means of Mantel tests. Results indicate that correlation and covariance structure in our species is stable, and that among-group correlation/covariance similarity is not related to genetic or phenotypic distance. Conversely, genetic and morphological distance matrices were highly correlated. Correlation and covariation patterns were largely associated with functional and developmental factors, which probably account for the stability of covariance patterns.     

The relative importance of plasticity versus genetic differentiation in explaining between population differences; a meta‐analysis

Both plasticity and genetic differentiation can contribute to phenotypic differences between populations. Using data on non‐fitness traits from reciprocal transplant studies, we show that approximately 60% of traits exhibit co‐gradient variation whereby genetic differences and plasticity‐induced differences between populations are the same sign. In these cases, plasticity is about twice as important as genetic differentiation in explaining phenotypic divergence. In contrast to fitness traits, the amount of genotype by environment interaction is small. Of the 40% of traits that exhibit counter‐gradient variation the majority seem to be hyperplastic whereby non‐native individuals express phenotypes that exceed those of native individuals. In about 20% of cases plasticity causes non‐native phenotypes to diverge from the native phenotype to a greater extent than if plasticity was absent, consistent with maladaptive plasticity. The degree to which genetic differentiation versus plasticity can explain phenotypic divergence varies a lot between species, but our proxies for motility and migration explain little of this variation.     

Genetics, development and evolution of adaptive pigmentation in vertebrates

The study of pigmentation has played an important role in the intersection of evolution, genetics, and developmental biology. Pigmentation's utility as a visible phenotypic marker has resulted in over 100 years of intense study of coat color mutations in laboratory mice, thereby creating an impressive list of candidate genes and an understanding of the developmental mechanisms responsible for the phenotypic effects. Variation in color and pigment patterning has also served as the focus of many classic studies of naturally occurring phenotypic variation in a wide variety of vertebrates, providing some of the most compelling cases for parallel and convergent evolution. Thus, the pigmentation model system holds much promise for understanding the nature of adaptation by linking genetic changes to variation in fitness-related traits. Here, I first discuss the historical role of pigmentation in genetics, development and evolutionary biology. I then discuss recent empirically based studies in vertebrates, which rely on these historical foundations to make connections between genotype and phenotype for ecologically important pigmentation traits. These studies provide insight into the evolutionary process by uncovering the genetic basis of adaptive traits and addressing such long-standing questions in evolutionary biology as (1) are adaptive changes predominantly caused by mutations in regulatory regions or coding regions? (2) is adaptation driven by the fixation of dominant mutations? and (3) to what extent are parallel phenotypic changes caused by similar genetic changes? It is clear that coloration has much to teach us about the molecular basis of organismal diversity, adaptation and the evolutionary process.     

QUANTITATIVE GENETICS OF HETEROCHRONY

A model of quantitative-genetic variation in developmental processes is introduced and analyzed. The model is of a bifurcating sequence of events in which traits develop from the same tissue until a transition occurs, after which they develop partially independently. Genetic and environmental variation in both the rates of tissue growth and in the timing of transitions is considered. The model shows how genetic variation in developmental parameters governs variation and covariation in phenotypic traits and how selection on the phenotype alters the distributions of developmental parameters. Particular attention is paid to the conditions under which selection will lead to changes in the average times of developmental events.     

Hsp90 inhibition and the expression of phenotypic variability in the rainforest species Drosophila birchii

Recently a heat shock protein (Hsp90) has been implicated as controlling the expression of cryptic genetic variation through buffering developmental processes. The release of variability in canalized characters following Hsp90 inhibition has been established in model species including Drosophila melanogaster and Arabidopsis thaliana , but has not yet been examined in species with limited distributions. To test if Hsp90 has a role in releasing phenotypic variation in rainforest Drosophila species, developing larvae from a large (> 1000 individuals) outbred population of Drosophila birchii were treated with the Hsp90 inhibitors geldanamycin and radicicol, and morphological traits, desiccation resistance, and life-history traits were measured. The means of all traits were influenced by inhibition. Although only the phenotypic variances of two canalized bristle traits were affected consistently, variability for two of the continuously varying traits (fecundity and development time) were also affected, albeit inconsistently. There was also no effect of Hsp90 inhibition on the developmental stability of the morphological traits as measured by fluctuating asymmetry. Hsp90 inhibition did not increase phenotypic variability in desiccation resistance, a trait previously shown to represent an evolutionary limit in this species. These results question the extent to which Hsp90 buffers variation for both quantitative and discrete traits, and highlight the need for further empirical studies to determine the involvement of Hsp90 in canalization and developmental stability. Nevertheless the results demonstrated increased variability in canalized traits, consistent with observations in model systems. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 457–465.     

A framework for the study of genetic variation in migratory behaviour

Evolutionary change results from selection acting on genetic variation. For migration to be successful, many different aspects of an animal’s physiology and behaviour need to function in a co-coordinated way. Changes in one migratory trait are therefore likely to be accompanied by changes in other migratory and life-history traits. At present, we have some knowledge of the pressures that operate at the various stages of migration, but we know very little about the extent of genetic variation in various aspects of the migratory syndrome. As a consequence, our ability to predict which species is capable of what kind of evolutionary change, and at which rate, is limited. Here, we review how our evolutionary understanding of migration may benefit from taking a quantitative-genetic approach and present a framework for studying the causes of phenotypic variation. We review past research, that has mainly studied single migratory traits in captive birds, and discuss how this work could be extended to study genetic variation in the wild and to account for genetic correlations and correlated selection. In the future, reaction-norm approaches may become very important, as they allow the study of genetic and environmental effects on phenotypic expression within a single framework, as well as of their interactions. We advocate making more use of repeated measurements on single individuals to study the causes of among-individual variation in the wild, as they are easier to obtain than data on relatives and can provide valuable information for identifying and selecting traits. This approach will be particularly informative if it involves systematic testing of individuals under different environmental conditions. We propose extending this research agenda by using optimality models to predict levels of variation and covariation among traits and constraints. This may help us to select traits in which we might expect genetic variation, and to identify the most informative environmental axes. We also recommend an expansion of the passerine model, as this model does not apply to birds, like geese, where cultural transmission of spatio-temporal information is an important determinant of migration patterns and their variation.