Iteroparous organisms maximize their overall fitness by optimizing their reproductive effort over multiple reproductive events. Hence, changes in reproductive effort are expected to have both short-and long-term consequences on parents and their offspring. In laboratory rodents, manipulation of reproductive efforts during lactation has however revealed few shortterm reproductive adjustments, suggesting that female laboratory rodents express maximal rather than optimal levels of reproductive investment as observed in semelparous organisms. Using a litter size manipulation (LSM) experiment in a small wild-derived rodent (the common vole; Microtus arvalis), we show that females altered their reproductive efforts in response to LSM, with females having higher metabolic rates and showing alternative body mass dynamics when rearing an enlarged rather than reduced litter. Those differences in female reproductive effort were nonetheless insufficient to fully match their pups' energy demand, pups being lighter at weaning in enlarged litters. Interestingly, female reproductive effort changes had longterm consequences, with females that had previously reared an enlarged litter being lighter at the birth of their subsequent litter and producing lower quality pups. We discuss the significance of using wild-derived animals in studies of reproductive effort optimization.
Behavior and metabolism are frontline reactions to environmental challenges that can covary in their response through at least two mechanisms. First, natural selection can generate correlation in phenotype among distinct populations if they are exposed to a common selective force. Thus, metabolism and behavior can exhibit phenotypic correlation among populations when responding (independently from each other) to co-varying selective forces. Second, because behavioral responses are energy-demanding, variation in energy acquisition or allocation among individuals of the same population can also generate, respectively, a positive or negative correlation within populations. To address this issue, we investigated among-and within-population (co)variations in exploration activity (EA) and resting metabolic rate (RMR) of adult common voles (Microtus arvalis) issued from four highelevation populations (> 1400 m a.s.l.) and five low-elevation populations (< 520 m a.s.l.). Individuals were acclimatized for at least 1 month to the same laboratory conditions before being tested for EA and RMR. Voles from high-elevation populations were more explorative and they had higher RMR than their counterparts from low-elevation populations. The similar effects of elevation on EA and RMR accounted for a correlation of 0.28 (0.064; 0.658) between EA and RMR across low-and highelevation populations. We found no evidence of a within-population correlation between EA and RMR. More work relying, for instance, on repeated sampling or experimental selection is nonetheless needed to confirm a lack of integration between metabolism and behavior at the individual level. Our results highlight the importance of co-varying selective forces in generating among-population phenotypic correlation between EA and RMR in this small rodent species. Significance statement There is increasing interest at deciphering the sources of covariation between metabolism and behavioral traits. Phenotypic covariation can be observed among populations if metabolism and behavior are responding independently from each other to covarying selective forces. Because behavioral responses are energy-demanding, variation in energy acquisition or allocation between individuals of the same population can also lead to, respectively, a positive or negative phenotypic correlation. In this study, we highlight the importance of co-varying selective forces in generating phenotypic correlation between metabolism and behavior across low-and high-elevation populations of a small rodent species. We found no evidence of a correlation within populations. More work relying, for instance, on repeated sampling or experimental selection is now needed to confirm a lack of integration between metabolism and behavior at the individual level.
A key adaptation of mammals to their environment is their ability to maintain a constant high body temperature, even at rest, under a wide range of ambient temperatures. In cold climates, this is achieved by an adaptive production of endogenous heat, known as nonshivering thermogenesis (NST), in the brown adipose tissue (BAT). This organ, unique to mammals, contains a very high density of mitochondria, and BAT correct functioning relies on the correct functioning of its mitochondria. Mitochondria enclose proteins encoded both in the maternally inherited mitochondrial genome and in the biparentally inherited nuclear genome, and one overlooked hypothesis is that both genomes and their interaction may shape NST. By housing under standardized conditions wild-derived common voles (Microtus arvalis) from two distinct evolutionary lineages (Western [W] and Central [C]), we show that W voles had greater NST than C voles. By introgressing those two lineages over at least nine generations, we then experimentally tested the influence of the nuclear and mitochondrial genomes on NST and related phenotypic traits. We found that between-lineage variation in NST and BAT size were significantly influenced by the mitochondrial and nuclear genomes, respectively, with the W mitochondrial genotype being associated with higher NST and the W nuclear genotype with a larger BAT. There were significant mito-nuclear interactions on whole animal body weight and resting metabolic rate (RMR). Hybrid voles were lighter and had higher RMR. Overall, our findings turn new light on the influence of the mitochondrial and nuclear genomes on thermogenesis and building adaptation to the environment in mammals.
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