Comparative Evolutionary Analysis of Metabolism in Nine Drosophila Species

Clark, Andrew G.; Wang, Lei

doi:10.2307/2410381

Cited by 14 publications

(7 citation statements)

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“…We found a high number of positive correlations, including the enzyme glycogen phosphorylase (GP), TR and HK as predicted from interspecific and intraspecific studies Skandalis and Darveau, 2012), but also the activity of other glycolytic enzymes (PGI and pyruvate kinase) and the mitochondrial enzyme CS. These results suggest that individuals with high metabolic rate show an overall increase in enzyme content, at least in workers, supporting the hypothesis that metabolic enzymes may form a correlated suite (Clark and Wang, 1994). In previous work on the same species we found that metabolic rate correlated with the activity of TR and HK but not PGI (Skandalis and Darveau, 2012), but variation among multiple colonies or even experimental variation in activity estimates could explain these differences.…”

Section: Determinants Of Individual Flight Energeticssupporting

confidence: 85%

“…Such patterns must arise from variation within a species and evolutionary mechanisms acting on such variation (Bennett, 1987;Clark and Wang, 1994). Within a bumblebee species (Bombus impatiens), individuals with larger wings had lower wingbeat frequency during flight, metabolic rate was positively correlated with wingbeat frequency, and the activity of some flight muscle enzymes positively correlated with metabolic rate (Skandalis and Darveau, 2012).…”

Section: Introductionmentioning

confidence: 99%

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Intraspecific variation in flight metabolic rate in the bumblebeeBombus impatiens: repeatability and functional determinants in workers and drones

Darveau

Billardon

Bélanger

2013

Journal of Experimental Biology

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The evolution of flight energetics requires that phenotypes be variable, repeatable and heritable. We studied intraspecific variation in flight energetics in order to assess the repeatability of flight metabolic rate and wingbeat frequency, as well as the functional basis of phenotypic variation in workers and drones of the bumblebee species Bombus impatiens. We showed that flight metabolic rate and wingbeat frequency were highly repeatable in workers, even when controlling for body mass variation using residual analysis. We did not detect significant repeatability in drones, but a smaller range of variation might have prevented us from finding significant values in our sample. Based on our results and previous findings, we associated the high repeatability of flight phenotypes in workers to the functional links between body mass, thorax mass, wing size, wingbeat frequency and metabolic rate. Moreover, differences between workers and drones were as predicted from these functional associations, where drones had larger wings for their size, lower wingbeat frequency and lower flight metabolic rate. We also investigated thoracic muscle metabolic phenotypes by measuring the activity of carbohydrate metabolism enzymes, and we found positive correlations between mass-independent metabolic rate and the activity of all enzymes measured, but in workers only. When comparing workers and drones that differ in flight metabolic rate, only the activity of the enzymes hexokinase and trehalase showed the predicted differences. Overall, our study indicates that there should be correlated evolution among physiological phenotypes at multiple levels of organization and morphological traits associated with flight.

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Section: Determinants Of Individual Flight Energeticssupporting

confidence: 85%

Section: Introductionmentioning

confidence: 99%

Intraspecific variation in flight metabolic rate in the bumblebeeBombus impatiens: repeatability and functional determinants in workers and drones

Darveau

Billardon

Bélanger

2013

Journal of Experimental Biology

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“…We adapted the colorimetric, kinetic ADH enzyme assay described in Clark and Wang (1994), and controlled for variation in the total amount of protein present in any given homogenate via a Bradford assay (see Supplemental Material). At the end of data collection, each test genotype (15 founders and 1737 RILs) was assigned a mean normalized ADH activity measure based on an average on 8.08 biological and technical assay replicates.…”

Section: Phenotyping Alcohol Dehydrogenase (Adh) Enzyme Activitymentioning

confidence: 99%

Genetic dissection of a model complex trait using the Drosophila Synthetic Population Resource

King¹,

Merkes²,

McNeil³

et al. 2012

Genome Res.

211

415

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Genetic dissection of complex, polygenic trait variation is a key goal of medical and evolutionary genetics. Attempts to identify genetic variants underlying complex traits have been plagued by low mapping resolution in traditional linkage studies, and an inability to identify variants that cumulatively explain the bulk of standing genetic variation in genome-wide association studies (GWAS). Thus, much of the heritability remains unexplained for most complex traits. Here we describe a novel, freely available resource for the Drosophila community consisting of two sets of recombinant inbred lines (RILs), each derived from an advanced generation cross between a different set of eight highly inbred, completely resequenced founders. The Drosophila Synthetic Population Resource (DSPR) has been designed to combine the high mapping resolution offered by multiple generations of recombination, with the high statistical power afforded by a linkage-based design. Here, we detail the properties of the mapping panel of >1600 genotyped RILs, and provide an empirical demonstration of the utility of the approach by genetically dissecting alcohol dehydrogenase (ADH) enzyme activity. We confirm that a large fraction of the variation in this classic quantitative trait is due to allelic variation at the Adh locus, and additionally identify several previously unknown modest-effect trans-acting QTL (quantitative trait loci). Using a unique property of multiparental linkage mapping designs, for each QTL we highlight a relatively small set of candidate causative variants for follow-up work. The DSPR represents an important step toward the ultimate goal of a complete understanding of the genetics of complex traits in the Drosophila model system.

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“…We were particularly interested in whether such an association might occur for one step in particular, HK, as occurs in orchid bee species ), or whether metabolic enzymes might form a correlated suite (Clark and Wang 1994). Only one enzyme, HK, decreases with increasing body size (figs.…”

Section: Interindividual Variation In Flight Muscle Metabolic Phenotypementioning

confidence: 99%

“…However, the strong correlation of these parameters between species need not be solely the result of evolution but could be the result of intraspecific scaling and an inherent plasticity of metabolic phenotypes. Thus, an important step is to ascertain to what extent similar relationships are observed intraspecifically (Bennett 1987;Clark and Wang 1994) and ultimately give rise to macrophysiological patterns.…”

Section: Introductionmentioning

confidence: 99%

Morphological and Physiological Idiosyncrasies Lead to Interindividual Variation in Flight Metabolic Rate in Worker Bumblebees (Bombus impatiens)

Skandalis

Darveau

2012

Physiological and Biochemical Zoology

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Although intraspecific variation in metabolic rate is associated with variation in body size, similarly sized individuals nonetheless vary greatly. At similar masses, hovering bumblebee workers (Bombus impatiens) can differ in metabolic rate up to twofold. We examined how such interindividual variation arises by studying covariation of flight metabolic rate with morphological and other physiological parameters. Body size alone explained roughly half the variation in flight metabolic rate. The remaining variation could be explained as the outcome of variation in wing morphology and possibly an association with variation in flight muscle metabolic enzyme activities. As shown using statistical models, for a given mass, higher metabolic rate was correlated with both higher thoracic temperature and higher wing stroke frequency, in turn resulting from smaller wing surface area. When organismal and cellular metabolism for a given mass were linked, variation in metabolic rate was positively correlated with the activities of trehalase and hexokinase. Altogether, covariation with morphology and other physiological parameters explains up to 75% of the variation in metabolic rate. We also investigated the role of flight experience and show that neither flight restriction nor the number of lifetime flights affected flight energetics or flight muscle phenotype. Additionally, manipulating the level of wing asymmetry increased flight wing stroke frequency, metabolic rate, and thoracic temperature, but it did not alter enzyme activity. We conclude that idiosyncrasies in body morphology largely explained interindividual variation in flight metabolic rate but flight muscle metabolic phenotype shows little variation associated with differences in flight experience.

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Comparative Evolutionary Analysis of Metabolism in Nine Drosophila Species

Cited by 14 publications

References 0 publications

Intraspecific variation in flight metabolic rate in the bumblebeeBombus impatiens: repeatability and functional determinants in workers and drones

Intraspecific variation in flight metabolic rate in the bumblebeeBombus impatiens: repeatability and functional determinants in workers and drones

Genetic dissection of a model complex trait using the Drosophila Synthetic Population Resource

Morphological and Physiological Idiosyncrasies Lead to Interindividual Variation in Flight Metabolic Rate in Worker Bumblebees (Bombus impatiens)

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