Marta K. Labocha

Morphometric indices of body condition in birds: a review

Morphometric estimates of body condition are widely used by ornithologists, but which estimates work best is a matter of debate. We review morphometric approaches (body mass, ratio and residual condition indices, predictive regression models, fat scoring, and abdominal profiles) for estimating body condition (defined as fat mass) in birds. We describe the strengths and weaknesses of each approach. Across diverse indices and species (~200 estimates total), the mean r2 relating condition indices to mass of body fat was 0.55, and 64% of the r2 values were greater than 0.50. But despite their generally good performance, condition indices sometimes perform poorly (i.e., r2 is low). The data indicate that: (1) no single index was clearly best, (2) on average body mass alone, fat scores, and predictive multiple regression equations explained slightly more than 50% of the variation in fat content, (3) on average, ratio and residual indices explained slightly less than 50% of the variation in fat content, and (4) body mass alone, a variable that can be easily and reliably measured, is as good or nearly as good an indicator of fat content as any other condition index. We recommend that: (1) morphometric indicators of condition be empirically validated, (2) researchers publish their body composition data in sufficient detail that they can be used in future analyses exploring the relative merits of different condition indices, and (3) multiple regression directly on measured traits be used instead of condition indices whenever the condition index is not empirically validated.ZusammenfassungMorphometrische Parameter zur Indikation der Körperkondition sind unter Ornithologen weit verbreitet, doch welche Parameter am Besten geeignet sind, wird lebhaft diskutiert. Wir stellen hier morphometrische Ansätze zur Indikation der Körperkondition, definiert als Fettmasse, bei Vögeln zusammen (Körpermasse, residuale Konditionsindices, Regressionsmodelle, Fettwert-Schätzungen und abdominales Pofil). Wir beschreiben die Stärken und Schwächen jedes dieser Ansätze. Über die verschiedenen Indices und Arten (insgesamt ~200 Ansätze) hinweg betrug das mittlere Bestimmtheitsmaß R2 zwischen Konditionsindices und Körpermasse 0,55, und 64% der R2-Werte waren größer als 0,50. Aber ungeachtet ihrer grundsätzlich ganz guten Bedeutung sind Konditionsindices manchmal sehr schwach (R2 ist gering). Die Daten deuten an, dass (1) kein Index für sich allein am besten war, (2) insgesamt Körpermasse, Fettwert und Regressionsmodelle etwas mehr als 50% der Variation im Fettgehalt erklärten, (3) im allgemeinen Verhältnisse und residuale Indices weniger als 50% der Variation im Fettgehalt erklärten, und (4) Körpermasse allein, eine leicht und zuverlässig zu bestimmende Größe, nahezu so gut ist als Indikator für den Fettgehalt wie jeder andere Konditionsindex. Wir empfehlen, dass (1) morphometrische Indikatoren der Körperkondition empirisch validiert werden, (2) Forscher ihre Daten zur Körperzusammensetzung so detailliert veröffentlichen, dass sie in zukünftigen Analysen verwendet werden können, um die relative Bedeutung der verschiedenen Konditionsindices überprüfen zu können, und (3) multiple Regressionsanalysen basierend auf den gemessenen Eigenschaften verwendet werden und nicht Konditionsindices, sofern diese nicht empirisch validiert sind.

GENETIC CORRELATIONS BETWEEN BASAL AND MAXIMUM METABOLIC RATES IN A WILD RODENT: CONSEQUENCES FOR EVOLUTION OF ENDOTHERMY

Abstract According to the aerobic capacity model, endothermy in birds and mammals evolved as a correlated response to selection for an ability of sustained locomotor activity, rather than in a response to direct selection for thermoregulatory capabilities. A key assumption of the model is that aerobic capacity is functionally linked to basal metabolic rate (BMR). The assumption has been tested in several studies at the level of phenotypic variation among individuals or species, but none has provided a clear answer whether the traits are genetically correlated. Here we present results of a genetic analysis based on measurements of the basal and the maximum swim‐ and cold‐induced oxygen consumption in about 1000 bank voles from six generations of a laboratory colony, reared from animals captured in the field. Narrow sense heritability (h2) was about 0.5 for body mass, about 0.4 for mass‐independent basal and maximum metabolic rates, and about 0.3 for factorial aerobic scopes. Dominance genetic and common environmental (5 maternal) effects were not significant. Additive genetic correlation between BMR and the swim‐induced aerobic capacity was high and positive, whereas correlation resulting from specific‐environmental effects was negative. However, BMR was not genetically correlated with the cold‐induced aerobic capacity. The results are consistent with the aerobic capacity model of the evolution of endothermy in birds and mammals.

Individual variation and repeatability of basal metabolism in the bank vole, Clethrionomys glareolus

Basal metabolic rate (BMR) is a fundamental energetic trait and has been measured in hundreds of birds and mammals. Nevertheless, little is known about the consistency of the population–average BMR or its repeatability at the level of individual variation. Here, we report that average mass–independent BMR did not differ between two generations of bank voles or between two trials separated by one month. Individual differences in BMR were highly repeatable across the one month interval: the coefficient of intraclass correlation was 0.70 for absolute log–transformed values and 0.56 for mass–independent values. Thus, BMR can be a meaningful measure of an individual physiological characteristic and can be used to test hypotheses concerning relationships between BMR and other traits. On the other hand, mass–independent BMR did not differ significantly across families, and the coefficient of intraclass correlation for full sibs did not differ from zero, which suggests that heritability of BMR in voles is not high.

Genetic variances and covariances of aerobic metabolic rates in laboratory mice

The genetic variances and covariances of traits must be known to predict how they may respond to selection and how covariances among them might affect their evolutionary trajectories. We used the animal model to estimate the genetic variances and covariances of basal metabolic rate (BMR) and maximal metabolic rate (MMR) in a genetically heterogeneous stock of laboratory mice. Narrow-sense heritability (h2) was approximately 0.38 ± 0.08 for body mass, 0.26 ± 0.08 for whole-animal BMR, 0.24 ± 0.07 for whole-animal MMR, 0.19 ± 0.07 for mass-independent BMR, and 0.16 ± 0.06 for mass-independent MMR. All h2 estimates were significantly different from zero. The phenotypic correlation of whole animal BMR and MMR was 0.56 ± 0.02, and the corresponding genetic correlation was 0.79 ± 0.12. The phenotypic correlation of mass-independent BMR and MMR was 0.13 ± 0.03, and the corresponding genetic correlation was 0.72 ± 0.03. The genetic correlations of metabolic rates were significantly different from zero, but not significantly different from one. A key assumption of the aerobic capacity model for the evolution of endothermy is that BMR and MMR are linked. The estimated genetic correlation between BMR and MMR is consistent with that assumption, but the genetic correlation is not so high as to preclude independent evolution of BMR and MMR.

Genetic Correlations in a Wild Rodent: Grass-Eaters and Fast-Growers Evolve High Basal Metabolic Rates

Basal metabolic rate (BMR), commonly used as a measure of the cost of living, is highly variable among species, and sources of the variation are subject to an enduring debate among comparative biologists. One of the hypotheses links the variation in BMR with diversity of food habits and life-history traits. We test this hypothesis by asking how BMR of a particular species, the bank vole Myodes (= Clethrionomys) glareolus, would change under selection for high growth rate (measured as a postweaning body mass change; MDPW) and the ability to cope with a low-quality herbivorous diet (measured as body mass change during a four-day test; MDLQD). We show that both of the traits are heritable in the narrow sense (MDPW: h2 = 0.30; MDLQD: h2 = 0.19), and are genetically correlated with mass-independent BMR (additive genetic correlation, rA = 0.28 for MDPW and 0.37 for MDLQD). Thus, both of the traits could change in response to a selection, and the selection would also result in a correlated evolution of the level of metabolism. The results are consistent with the hypothesis that a part of the interspecific variation in BMR evolved in response to selection for life-history and ecological traits such as food habits.

Systematic profiling of Caenorhabditis elegans locomotive behaviors reveals additional components in G-protein Gαq signaling

Genetic screens have been widely applied to uncover genetic mechanisms of movement disorders. However, most screens rely on human observations of qualitative differences. Here we demonstrate the application of an automatic imaging system to conduct a quantitative screen for genes regulating the locomotive behavior in Caenorhabditis elegans. Two hundred twenty-seven neuronal signaling genes with viable homozygous mutants were selected for this study. We tracked and recorded each animal for 4 min and analyzed over 4,400 animals of 239 genotypes to obtain a quantitative, 10-parameter behavioral profile for each genotype. We discovered 87 genes whose inactivation causes movement defects, including 50 genes that had never been associated with locomotive defects. Computational analysis of the high-content behavioral profiles predicted 370 genetic interactions among these genes. Network partition revealed several functional modules regulating locomotive behaviors, including sensory genes that detect environmental conditions, genes that function in multiple types of excitable cells, and genes in the signaling pathway of the G protein Gαq, a protein that is essential for animal life and behavior. We developed quantitative epistasis analysis methods to analyze the locomotive profiles and validated the prediction of the γ isoform of phospholipase C as a component in the Gαq pathway. These results provided a system-level understanding of how neuronal signaling genes coordinate locomotive behaviors. This study also demonstrated the power of quantitative approaches in genetic studies.

CONTEST WINNING AND METABOLIC COMPETENCE IN MALE BANK VOLES CLETHRIONOMYS GLAREOLUS

Famale bank voles prefer dominant males as mates, and it has been suggested that this preference may benefit females genetically, via increased fitness of their progeny. This requires that male ability to win intrasexual contests is associated with their genetic quality. An important aspect of individual quality is metabolic competence. Here, we investigated whether male ability to win contests is correlated with aerobic capacity (the maximum rate of oxygen consumption) or factorial aerobic scope (the ratio of aerobic capacity to basal metabolic rate [BMR]). The ability to win was assessed as proportion of dominant behaviours in staged contests with five other males, and aerobic capacity was measured both during exercise (swimming) and during cold-exposure trials. Contest winning ability was not correlated with the aerobic capacity (p > 0.6), the factorial metabolic scope (p > 0.25) or BMR (p = 0.24; all the traits were corrected for the effect of body mass). Thus, the results indicate that the trait (male dominance) subject to female preference in the bank vole fails to reveal an important aspect of male quality, i.e. his metabolic competence.

A strong response to selection on mass-independent maximal metabolic rate without a correlated response in basal metabolic rate

Metabolic rates are correlated with many aspects of ecology, but how selection on different aspects of metabolic rates affects their mutual evolution is poorly understood. Using laboratory mice, we artificially selected for high maximal mass-independent metabolic rate (MMR) without direct selection on mass-independent basal metabolic rate (BMR). Then we tested for responses to selection in MMR and correlated responses to selection in BMR. In other lines, we antagonistically selected for mice with a combination of high mass-independent MMR and low mass-independent BMR. All selection protocols and data analyses included body mass as a covariate, so effects of selection on the metabolic rates are mass adjusted (that is, independent of effects of body mass). The selection lasted eight generations. Compared with controls, MMR was significantly higher (11.2%) in lines selected for increased MMR, and BMR was slightly, but not significantly, higher (2.5%). Compared with controls, MMR was significantly higher (5.3%) in antagonistically selected lines, and BMR was slightly, but not significantly, lower (4.2%). Analysis of breeding values revealed no positive genetic trend for elevated BMR in high-MMR lines. A weak positive genetic correlation was detected between MMR and BMR. That weak positive genetic correlation supports the aerobic capacity model for the evolution of endothermy in the sense that it fails to falsify a key model assumption. Overall, the results suggest that at least in these mice there is significant capacity for independent evolution of metabolic traits. Whether that is true in the ancestral animals that evolved endothermy remains an important but unanswered question.

WormGender – Open-Source Software for Automatic Caenorhabditis elegans Sex Ratio Measurement

Fast and quantitative analysis of animal phenotypes is one of the major challenges of current biology. Here we report the WormGender open-source software, which is designed for accurate quantification of sex ratio in Caenorhabditis elegans. The software functions include, i) automatic recognition and counting of adult hermaphrodites and males, ii) a manual inspection feature that enables manual correction of errors, and iii) flexibility to use new training images to optimize the software for different imaging conditions. We evaluated the performance of our software by comparing manual and automated assessment of sex ratio. Our data showed that the WormGender software provided overall accurate sex ratio measurements. We further demonstrated the usage of WormGender by quantifying the high incidence of male (him) phenotype in 27 mutant strains. Mutants of nine genes (brc-1, C30G12.6, cep-1, coh-3, him-3, him-5, him-8, skr-1, unc-86) showed significant him phenotype. The WormGender is written in Java and can be installed and run on both Windows and Mac platforms. The source code is freely available together with a user manual and sample data at http://www.QuantWorm.org/. The source code and sample data are also available at http://dx.doi.org/10.6084/m9.figshare.1541248.

Age-specific decline in take-off flight performance in a small passerine

Age-specific differences in individual performance are reported in a number of taxa and are particularly well documented in humans. However, such data are generally lacking for birds, the taxon showing exceptionally long life in relation to body size. Here, we studied differences in vertical flight performance among three distinctive age classes (0.5-, 2- and 4.5-year-old birds) in laboratory-kept zebra finches, Taeniopygia guttata . We found that take-off flight speed differed significantly between the age classes with the oldest birds being ca. 10% slower than the youngest birds. Age classes also differed significantly in flight motivation, with old birds tending to be less motivated to fly than young ones. Thus, the age-specific decline in flight performance is clearly visible in zebra finches. In a broader perspective, poorer flight performance may impair foraging efficiency, social interactions and, most importantly, take-off speed when escaping predators. This may help elucidate age-specific decline in reproductive and survival rates commonly observed in natural populations.