MHC influences infection with parasites and winter survival in the root vole Microtus oeconomus

Selective pressure from parasites is thought to maintain the polymorphism of major histocompatibility complex (MHC) genes. Although a number of studies have shown a relationship between the MHC and parasitic infections, the fitness consequences of such associations are less well documented. In the present paper, we characterised the variation in exon 2 of MHC class II DRB gene in the root vole and examined the effects of that gene on parasite prevalence and winter survival. We identified 18 unique exon 2 sequences, which translated into 10 unique amino acid sequences. Phylogenetic analysis revealed the presence of three distinct clusters, and allele distributions among these individuals suggested that the clusters correspond to three different loci. Although the rate of synonymous substitutions (dS) exceeded the rate of nonsynonymous substitutions (dN) across sequences, implying purifying selection, dN was significantly elevated at antigen-binding sites, suggesting that these sites could be under positive selection. Screening for parasites revealed a moderate prevalence of infection with gastrointestinal parasites (24 % infected), but a high infection rate for blood parasites (56 % infected). Infection with the blood parasite Babesia ssp. decreased survival almost twofold (25.7 vs. 13.9 %). Animals possessing the amino acid sequence AA*08 survived better than others (44.9 vs. 22 %), and they were infected with Babesia ssp. less often (13.9 vs 25.7 %). In contrast, individuals carrying allele AA*05 were infected more often (31.7 vs. 15.3 %). Heterozygosity at one of the putative loci was associated with a lower probability of infection with Babesia ssp., but at the other locus, the association was reversed. The unexpected latter result could be at least partly explained by the increased frequency of the susceptible allele AA*05 among heterozygotes. Overall, we demonstrate that infection with Babesia ssp. is a strong predictor of winter survival and that MHC genes are important predictors of infection status as well as survival in the root vole

The relationship between basal metabolic rate and daily energy expenditure in birds and mammals

We examined the relationship between daily energy expenditure (DEE) and basal metabolic rate (BMR) in birds and mammals. Two models of the relationship between DEE and BMR were distinguished: a ''shared pathways'' model in which DEE replaces BMR in the active organism and a ''partitioned pathways'' model in which DEE includes BMR-that is, BMR is separate from the metabolic pathways that result in activity metabolism (ACT), and DEE = ACT + BMR. The appropriate null hypotheses for the relationship between basal and active metabolism are r(DEE . BMR) = 0 and r(ACT . BMR) = 0, respectively. Correlations of the residuals (d and b) of the logarithms of DEE and BMR from their allometric regressions with the logarithm of body mass were tested against these null models. Using phylogenetically independent contrasts, we found no significant relationship between DEE and BMR in birds, but a strong relationship (r(db) = 0.86) among mammals. Thus, the hypothesis that sustained working capacity is related to basal metabolism is supported for mammals but not for birds. Residuals of metabolic variables from allometric regressions on body mass were greater for mammals than for birds and suggest that mammals are more diversified in their energetic physiology. The idea that sustainable energy expenditure may be pushed to physiological limits in mammals but not in birds is not supported, however, because the ratio of DEE to BMR has a somewhat lower mean and greater variance in mammals compared to birds. The nature of the relationship between DEE and BMR in mammals and the apparent absence of such a relationship in birds remain major puzzles in animal physiology

Brain size, gut size and cognitive abilities : the energy trade-offs tested in artificial selection experiment

The enlarged brains of homeotherms bring behavioural advantages, but also incur high energy expenditures. The ‘expensive brain’ (EB) hypothesis posits that the energetic costs of the enlarged brain and the resulting increased cognitive abilities (CA) were met by either increased energy turnover or reduced allocation to other expensive organs, such as the gut. We tested the EB hypothesis by analysing correlated responses to selection in an experimental evolution model system, which comprises line types of laboratory mice selected for high or low basal metabolic rate (BMR), maximum (VO2max) metabolic rates and random-bred (unselected) lines. The traits are implicated in the evolution of homeothermy, having been pre-requisites for the encephalization and exceptional CA of mammals, including humans. High-BMR mice had bigger guts, but not brains, than mice of other line types. Yet, they were superior in the cognitive tasks carried out in both reward and avoidance learning contexts and had higher neuronal plasticity (indexed as the long-term potentiation) than their counterparts. Our data indicate that the evolutionary increase of CA in mammals was initially associated with increased BMR and brain plasticity. It was also fuelled by an enlarged gut, which was not traded off for brain size

Determinants of intra-specific variation in basal metabolic rate

Basal metabolic rate (BMR) provides a widely accepted benchmark of metabolic expenditure for endotherms under laboratory and natural conditions. While most studies examining BMR have concentrated on inter-specific variation, relatively less attention has been paid to the determinants of within-species variation. Even fewer studies have analysed the determinants of within-species BMR variation corrected for the strong influence of body mass by appropriate means (e.g. ANCOVA). Here, we review recent advancements in studies on the quantitative genetics of BMR and organ mass variation, along with their molecular genetics. Next, we decompose BMR variation at the organ, tissue and molecular level. We conclude that within-species variation in BMR and its components have a clear genetic signature, and are functionally linked to key metabolic process at all levels of biological organization. We highlight the need to integrate molecular genetics with conventional metabolic field studies to reveal the adaptive significance of metabolic variation. Since comparing gene expressions inter-specifically is problematic, within-species studies are more likely to inform us about the genetic underpinnings of BMR. We also urge for better integration of animal and medical research on BMR; the latter is quickly advancing thanks to the application of imaging technologies and ‘omics’ studies. We also suggest that much insight on the biochemical and molecular underpinnings of BMR variation can be gained from integrating studies on the mammalian target of rapamycin (mTOR), which appears to be the major regulatory pathway influencing the key molecular components of BMR

To be or not to be.... a small

Body mass (size) is a very important biological character, interrelated with key life history traits, such as fertility, age at maturity, reproductive success and mortality. On the physiological level, body mass is also closely associated with key components of energy budgets. Yet, factors moulding within-species variation of body mass and its relations to energy expenditures and life history traits are still not fully understood. The weasel (Mustela nivalis Linneaus, 1776) is an extremely interesting species almost perfectly suited to study these relations. It is characterized by a considerable variation in body mass (range 40-150 g) and extremely high metabolic rates. This highly specialised predator hunts on different species of rodents. In the forest weasel preys on the bank vole (Clethionomys glareolus) and yellow-necked mouse (Apodemus flavicollis), whereas in the open habitats it mainly preys on the voles (Microtus spp.). Due to their small body size and high metabolic rates, weasels encounter numerous constraints. The prey size is one of the main ecological factors determining variation in weasel's body mass. Males heavier than 100 g suffer from increased winter mortality. We therefore hypothesise that in summer bigger males are favoured by sexual selection, whereas in winter energy constrains select for smaller animals. To test this we investigated time budgets, resting (RMR) and field metabolic rate (FMR) in weasel males of various sizes during winter and summer. In contrast to other carnivore species the body-mass corrected RMR of weasels was lower in winter than in summer. Weasels also minimised their winter energetic expenditures by decreasing hunting activity (on average 4 h/day in summer vs. less than 2 h/day in winter). Irrespective of body mass this was usually sufficient to catch just a single prey unit. In accordance with our expectations the winter hunting activity was sufficient to balance the energy budget of small males, but compromised survival prospects of bigger individuals

Mice selected for a high basal metabolic rate evolved larger guts but not more efficient mitochondria

International audienceIntra-specific variation in both the basal metabolic rate (BMR) and mitochondrial efficiency (the amount of ATP produced per unit of oxygen consumed) has profound evolutionary and ecological consequences. However, the functional mechanisms responsible for this variation are not fully understood. Mitochondrial efficiency is negatively correlated with BMR at the interspecific level but it is positively correlated with performance capacity at the intra-specific level. This discrepancy is surprising, as theories explaining the evolution of endothermy assume a positive correlation between BMR and performance capacity. Here, we quantified mitochondrial oxidative phosphorylation activity and efficiency in two lines of laboratory mice divergently selected for either high (H-BMR) or low (L-BMR) levels of BMR. H-BMR mice had larger livers and kidneys (organs that are important predictors of BMR). H-BMR mice also showed higher oxidative phosphorylation activity in liver mitochondria but this difference can be hypothesized to be a direct effect of selection only if the heritability of this trait is low. However, mitochondrial efficiency in all studied organs did not differ between the two lines. We conclude that the rapid evolution of BMR can reflect changes in organ size rather than mitochondrial properties, and does not need to be accompanied obligatorily by changes in mitochondrial efficiency