Geographical patterns of morphological variation have been useful in addressing hypotheses about environmental adaptation. In particular, latitudinal clines in phenotypes have been studied in a number of Drosophila species. Some environmental conditions along latitudinal clines – e.g. temperature – also vary along altitudinal clines, but these have been studied infrequently and it remains unclear whether these environmental factors are similar enough for convergence or parallel evolution. Most clinal studies in Drosophila have dealt exclusively with univariate phenotypes, allowing for the detection of clinal relationships, but not for estimating the directions of co-variation between them. We measured variation in wing shape and size in Drosophila melanogaster derived from populations at varying altitudes and latitudes across sub-Saharan Africa. Geometric morphometrics allows us to compare shape changes associated with latitude and altitude, and manipulating rearing temperature allows us to quantify the extent to which thermal plasticity recapitulates clinal effects. Comparing effect vectors demonstrates that altitude, latitude and temperature are only partly associated, and that the altitudinal shape effect may differ between Eastern and Western Africa. Our results suggest that selection responsible for these phenotypic clines may be more complex than just thermal adaptation.
Due to the complexity of genotype-phenotype relationships, simultaneous analyses of genomic associations with multiple traits will be more powerful and informative than a series of univariate analyses. However, in most cases, studies of genotypephenotype relationships have been analyzed only one trait at a time. Here, we report the results of a fully integrated multivariate genome-wide association analysis of the shape of the Drosophila melanogaster wing in the Drosophila Genetic Reference Panel. Genotypic effects on wing shape were highly correlated between two different laboratories. We found 2396 significant SNPs using a 5% false discovery rate cutoff in the multivariate analyses, but just four significant SNPs in univariate analyses of scores on the first 20 principal component axes. One quarter of these initially significant SNPs retain their effects in regularized models that take into account population structure and linkage disequilibrium. A key advantage of multivariate analysis is that the direction of the estimated phenotypic effect is much more informative than a univariate one. We exploit this fact to show that the effects of knockdowns of genes implicated in the initial screen were on average more similar than expected under a null model. A subset of SNP effects were replicable in an unrelated panel of inbred lines. Association studies that take a phenomic approach, considering many traits simultaneously, are an important complement to the power of genomics.
A fundamental question in evolutionary biology is the relative importance of selection and genetic architecture in determining evolutionary rates. Adaptive evolution can be described by the multivariate breeders' equation ( ), which predicts evolutionary change for a suite of phenotypic traits ( ) as a product of directional selection acting on them ( β ) and the genetic variance–covariance matrix for those traits ( G ). Despite being empirically challenging to estimate, there are enough published estimates of G and β to allow for synthesis of general patterns across species. We use published estimates to test the hypotheses that there are systematic differences in the rate of evolution among trait types, and that these differences are, in part, due to genetic architecture. We find some evidence that sexually selected traits exhibit faster rates of evolution compared with life-history or morphological traits. This difference does not appear to be related to stronger selection on sexually selected traits. Using numerous proposed approaches to quantifying the shape, size and structure of G , we examine how these parameters relate to one another, and how they vary among taxonomic and trait groupings. Despite considerable variation, they do not explain the observed differences in evolutionary rates.
Phenotypic integration and plasticity are central to our understanding of how complex phenotypic traits evolve. Evolutionary change in complex quantitative traits can be predicted using the multivariate breeders’ equation, but such predictions are only accurate if the matrices involved are stable over evolutionary time. Recent work, however, suggests that these matrices are temporally plastic, spatially variable and themselves evolvable. The data available on phenotypic variance-covariance matrix (P) stability is sparse, and largely focused on morphological traits. Here we compared P for the structure of the complex sexual advertisement call of six divergent allopatric populations of the Australian black field cricket, Teleogryllus commodus. We measured a subset of calls from wild-caught crickets from each of the populations and then a second subset after rearing crickets under common-garden conditions for three generations. In a second experiment, crickets from each population were reared in the laboratory on high- and low-nutrient diets and their calls recorded. In both experiments, we estimated P for call traits and used multiple methods to compare them statistically (Flury hierarchy, geometric subspace comparisons and random skewers). Despite considerable variation in means and variances of individual call traits, the structure of P was largely conserved among populations, across generations and between our rearing diets. Our finding that P remains largely stable, among populations and between environmental conditions, suggests that selection has preserved the structure of call traits in order that they can function as an integrated unit.
For a given gene, different mutations influence organismal phenotypes to varying degrees. However, the expressivity of these variants not only depends on the DNA lesion associated with the mutation, but also on factors including the genetic background and rearing environment. The degree to which these factors influence related alleles, genes, or pathways similarly, and whether similar developmental mechanisms underlie variation in the expressivity of a single allele across conditions and among alleles is poorly understood. Besides their fundamental biological significance, these questions have important implications for the interpretation of functional genetic analyses, for example, if these factors alter the ordering of allelic series or patterns of complementation. We examined the impact of genetic background and rearing environment for a series of mutations spanning the range of phenotypic effects for both the scalloped and vestigial genes, which influence wing development in Drosophila melanogaster. Genetic background and rearing environment influenced the phenotypic outcome of mutations, including intra-genic interactions, particularly for mutations of moderate expressivity. We examined whether cellular correlates (such as cell proliferation during development) of these phenotypic effects matched the observed phenotypic outcome. While cell proliferation decreased with mutations of increasingly severe effects, surprisingly it did not co-vary strongly with the degree of background dependence. We discuss these findings and propose a phenomenological model to aid in understanding the biology of genes, and how this influences our interpretation of allelic effects in genetic analysis.
BackgroundExtracting important descriptors and features from images of biological specimens is an ongoing challenge. Features are often defined using landmarks and semi-landmarks that are determined a priori based on criteria such as homology or some other measure of biological significance. An alternative, widely used strategy uses computational pattern recognition, in which features are acquired from the image de novo. Subsets of these features are then selected based on objective criteria. Computational pattern recognition has been extensively developed primarily for the classification of samples into groups, whereas landmark methods have been broadly applied to biological inference.ResultsTo compare these approaches and to provide a general community resource, we have constructed an image database of Drosophila melanogaster wings - individually identifiable and organized by sex, genotype and replicate imaging system - for the development and testing of measurement and classification tools for biological images. We have used this database to evaluate the relative performance of current classification strategies. Several supervised parametric and nonparametric machine learning algorithms were used on principal components extracted from geometric morphometric shape data (landmarks and semi-landmarks). For comparison, we also classified phenotypes based on de novo features extracted from wing images using several computer vision and pattern recognition methods as implemented in the Bioimage Classification and Annotation Tool (BioCAT).ConclusionsBecause we were able to thoroughly evaluate these strategies using the publicly available Drosophila wing database, we believe that this resource will facilitate the development and testing of new tools for the measurement and classification of complex biological phenotypes.Electronic supplementary materialThe online version of this article (doi:10.1186/s13742-015-0065-6) contains supplementary material, which is available to authorized users.
The evolution of acoustic behaviour and that of the morphological traits mediating its production are often coupled. Lack of variation in the underlying morphology of signalling traits has the potential to constrain signal evolution. This relationship is particularly likely in field crickets, where males produce acoustic advertisement signals to attract females by stridulating with specialized structures on their forewings. In this study, we characterise the size and geometric shape of the forewings of males from six allopatric populations of the black field cricket (Teleogryllus commodus) known to have divergent advertisement calls. We sample from each of these populations using both wild-caught and common-garden reared cohorts, allowing us to test for multivariate relationships between wing morphology and call structure. We show that the allometry of shape has diverged across populations. However, there was a surprisingly small amount of covariation between wing shape and call structure within populations. Given the importance of male size for sexual selection in crickets, the divergence we observe among populations has the potential to influence the evolution of advertisement calls in this species.
A fundamental question in evolutionary biology is the relative importance of selection and genetic architecture in determining evolutionary rates. Adaptive evolution can be described by the multivariate breeders' equation (Δz = Gβ), which predicts evolutionary change for a suite of phenotypic traits (Δz) as a product of directional selection acting on them (β) and the genetic variance-covariance matrix for those traits (G). Despite being empirically challenging to estimate, there are enough published estimates ofGandβto allow for synthesis of general patterns across species. We use published estimates to test the hypotheses that there are systematic differences in the rate of evolution among trait types, and that these differences are in part due to genetic architecture. We find evidence that sexually selected traits exhibit faster rates of evolution compared to life-history or morphological traits. This difference does not appear to be related to stronger selection on sexually selected traits. Using numerous proposed approaches to quantifying the shape, size and structure ofGwe examine how these parameters relate to one another, and how they vary among taxonomic and trait groupings. Despite considerable variation, they do not explain the observed differences in evolutionary rates.
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