[Show abstract][Hide abstract] ABSTRACT: In social species, the hierarchical status of an individual has important consequences for its fitness. While many studies have focused on individual condition to explain access to dominance, very few have investigated the influence of the social environment, especially during early life. Yet it is known that environmental conditions early in life may influence several traits at adulthood. Here, we examine the influence of early social environment on accession to dominance by investigating the influence of litter size and sex composition on survival and the probability of ascending to dominance later in life using a 20-year dataset from a wild population of Alpine marmots (Marmota marmota). Although litter size had no effect on the fate of individuals, litter sex composition affected male juvenile survival and both male and female probabilities of reaching dominant status when adult. Male juveniles incur lower survival when the number of male juveniles in the litter increases, and individuals of both sexes from male-biased litters are more likely to become dominant than individuals from female-biased litters. However, the absolute number of sisters in the litter, rather than the sex ratio, seems to be an important predictor of the probability of acquiring dominant status: pups having more sisters are less likely to become dominant. Several potential mechanisms to explain these results are discussed.
[Show abstract][Hide abstract] ABSTRACT: Studying the different roles of adaptive genes is still a challenge in evolutionary ecology and requires reliable genotyping of large numbers of individuals. Next-generation sequencing (NGS) techniques enable such large-scale sequencing, but stringent data processing is required. Here, we develop an easy to use methodology to process amplicon-based NGS data and we apply this methodology to reliably genotype four major histocompatibility complex (MHC) loci belonging to MHC class I and II of Alpine marmots (Marmota marmota). Our post-processing methodology allowed us to increase the number of retained reads. The quality of genotype assignment was further assessed using three independent validation procedures. A total of 3069 high-quality MHC genotypes were obtained at four MHC loci for 863 Alpine marmots with a genotype assignment error rate estimated as 0.21%. The proposed methodology could be applied to any genetic system and any organism, except when extensive copy-number variation occurs (that is, genes with a variable number of copies in the genotype of an individual). Our results highlight the potential of amplicon-based NGS techniques combined with adequate post-processing to obtain the large-scale highly reliable genotypes needed to understand the evolution of highly polymorphic functional genes.Heredity advance online publication, 11 March 2015; doi:10.1038/hdy.2015.13.
[Show abstract][Hide abstract] ABSTRACT: Although long neglected, female competition is widespread and may have stronger evolutionary consequences than previously thought. In singular breeders, reproductive success is conditional on social status, and intrasexual competition for the dominant position can be particularly severe in females. Because the ability of females to secure the dominant position may strongly influence their fitness, a better understanding of the determinants of dominance maintenance is needed. Using a 21-year data set on Alpine marmots, Marmota marmota, we investigated the potential drivers of female dominance loss in a singularly breeding mammal. Particularly, we tested whether the dominant females' ability to retain their social position depended on the number and the characteristics (age, relatedness to dominant individuals) of potential competitors in the social unit. To identify the potential underlying mechanism, we further investigated how the number of subordinate females affected females' competitive ability. We found that the risk of losing the dominant position increased with the number of subordinate adult females in the group, but that the age of the subordinate females and their parentage relationships to the dominant individuals were unlikely to be driving dominance loss in this species. Moreover, when the number of potential competitors in the social unit increased, we observed a difference in body mass increase between the dominant and her subordinates leading to a decrease in the body mass difference between dominant females and their subordinate adult females, and ultimately to a higher risk of females losing the dominant position. Overall, our results showed that the number of potential competitors in a social group affects the females' ability to secure their dominant position, and suggested that this effect is mediated through changes in female body mass.
[Show abstract][Hide abstract] ABSTRACT: The way that plants and animals respond to climate change varies widely among species, but the biological features underlying their actual response remains largely unknown. Here, from a 20-year monitoring study, we document a continuous decrease in litter size of the Alpine marmot (Marmota marmota) since 1990. To cope with harsh winters, Alpine marmots hibernate in burrows and their reproductive output should depend more on spring conditions compared to animals that are active year-round. However, we show that litter size decreased over time because of the general thinning of winter snow cover that has been repeatedly reported to occur in the Alps over the same period, despite a positive effect of an earlier snowmelt in spring. Our results contrast markedly with a recent study on North American yellow-bellied marmots, suggesting that between-species differences in life histories can lead to opposite responses to climate change, even between closely related species. Our case study therefore demonstrates the idiosyncratic nature of the response to climate change and emphasizes, even for related species with similar ecological niches, that it may be hazardous to extrapolate life history responses to climate change from one species to another.
[Show abstract][Hide abstract] ABSTRACT: Sex-specific senescence has been commonly reported in highly dimorphic and polygynous species. However, whether between-sex differences in senescence occur in monogamous and monomorphic species is poorly known. In this study, we used an extensive dataset of 20 years of mass measurements on free-ranging male and female Alpine marmots (Marmota marmota), a medium-sized, long-lived, social and hibernating mammal, to assess sex-specific patterns of senescence in body mass. We tested for the occurrence of both a decrease in body mass scaled to absolute age (called chronological senescence) and a decrease in body mass scaled to individual age at death (called terminal decline). Whereas males showed evidence of both chronological senescence and terminal decline in body mass, females did not show any detectable senescence in body mass. This unexpected between-sex difference of senescence in a species subject to weak sexual selection might be shaped either by costs of an asymmetric intra-sex competition for mates or by costs of social thermoregulation.
[Show abstract][Hide abstract] ABSTRACT: Movement is fundamental to individual and population dynamics, as it allows individuals to meet their basic requirements. Although movement patterns reflect interactions between internal and external factors, only few studies have examined the effects of these factors on movement simultaneously, and they generally focused on particular biological contexts (e.g. dispersal, foraging). However, the relative importance of these factors in driving individual routine movements might reflect a species' potential flexibility to cope with landscape changes and therefore buffer their potential impact on fitness. We used data from GPS collars on Scandinavian brown bears to investigate the relative role of these factors, as well as an additional factor (period of the year) on routine movements at two spatial scales (hourly and daily relocations). As expected, internal factors played a major role in driving movement, compared to external factors at both scales, but its relative importance was greater at a finer scale. In particular, the interaction between reproductive status and period of the year was one of the most influential variables, females being constrained by the movement capacity of their cubs in the first periods of the year. The effect of human disturbance on movement was also greater for females with cubs than for lone females. This study showed how reciprocal modulation of internal and external factors is shaping space use of brown bears. We stress that these factors should be studied simultaneously to avoid the risk of obtaining context-dependent inferences. Moreover, the study of their relative contribution is also highly relevant in the context of multiple-use landscapes, as human activities generally affect the landscape more than they affect the internal states of an individual. Species or individuals with important internal constraints should be less responsive to changes in their environment as they have less freedom from internal constraints and should thus be more sensitive to human alteration of the landscape, as shown for females with cubs in this study.
[Show abstract][Hide abstract] ABSTRACT: The major histocompatibility complex (MHC) genes code for proteins that play a critical role in the immune system response. The MHC genes are among the most polymorphic genes in vertebrates, presumably due to balancing selection. The two MHC classes appear to differ in the rate of evolution, but the reasons for this variation are not well understood. Here, we investigate the level of polymorphism and the evolution of sequences that code for the peptide-binding regions of MHC class I and class II DRB genes in the Alpine marmot (Marmota marmota). We found evidence for four expressed MHC class I loci and two expressed MHC class II loci. MHC genes in marmots were characterized by low polymorphism, as one to eight alleles per putative locus were detected in 38 individuals from three French Alps populations. The generally limited degree of polymorphism, which was more pronounced in class I genes, is likely due to bottleneck the populations undergone. Additionally, gene duplication within each class might have compensated for the loss of polymorphism at particular loci. The two gene classes showed different patterns of evolution. The most polymorphic of the putative loci, Mama-DRB1, showed clear evidence of historical positive selection for amino acid replacements. However, no signal of positive selection was evident in the MHC class I genes. These contrasting patterns of sequence evolution may reflect differences in selection pressures acting on class I and class II genes.
[Show abstract][Hide abstract] ABSTRACT: 1. Identification of suitable habitats for small, endangered populations is important to preserve key areas for potential augmentation. However, replicated spatial data from a sufficient number of individuals are often unavailable for such populations, leading to unreliable habitat models. This is the case for the endangered Pyrenean brown bear Ursus arctos population, with only about 20 individuals surviving in two isolated groups. 2. We conducted habitat suitability analyses at two spatial scales (coarse and local). Given the limited available data, we used information from the nearby Cantabrian brown bear population in Spain to develop a two-dimensional model (human and natural variables) at a coarse scale, based on logistic regression, which we applied in the Pyrenees. At a local scale, we used bear presence in the Pyrenees to describe the population's ecological niche and develop a habitat suitability model using presence-only methods. We combined these models to obtain a more integrative understanding of bear requirements. 3. The coarse-scale model showed a good transferability to the Pyrenees, identifying preference for areas with high forest connectivity, masting trees, rugged terrain and shrubs and avoidance of areas with anthropogenic structures. The local-scale model was consistent with the coarse-scale model. Bears showed a trade-off between food resources (scarcer at high elevations) and human presence (higher at low elevations). 4. Our models illustrated that there is unoccupied good habitat for bears in the Pyrenees that could host new individuals. Combining two scales allowed us to identify areas that should be prioritized for management actions and also those that should be easier to manage for bears. 5. Synthesis and applications. Our study illustrates how a nested-scale approach, combining coarse data from a different population and fine-scale local data, can aid in the management of small populations with limited data. This was applied to remnant brown bear populations to identify priorities for conservation management.
[Show abstract][Hide abstract] ABSTRACT: Paternity insurance and dominance tenure length are two important components of male reproductive success, particularly in species where reproduction is highly skewed towards a few individuals. Identifying the factors affecting these two components is crucial to better understand the pattern of variation in reproductive success among males. In social species, the social context (i.e. group size and composition) is likely to influence the ability of males to secure dominance and to monopolize reproduction. Most studies have analyzed the factors affecting paternity insurance and dominance tenure separately. We use a long term data set on Alpine marmots to investigate the effect of the number of subordinate males on both paternity insurance and tenure of dominant males. We show that individuals which are unable to monopolize reproduction in their family groups in the presence of many subordinate males are likely to lose dominance the following year. We also report that dominant males lose body mass in the year they lose both paternity and dominance. Our results suggest that controlling many subordinate males is energetically costly for dominant males, and those unable to support this cost lose the control over both reproduction and dominance. A large number of subordinate males in social groups is therefore costly for dominant males in terms of fitness.
PLoS ONE 01/2012; 7(1):e29508. DOI:10.1371/journal.pone.0029508 · 3.23 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Habitat preferences of alpine marmots, Marmota marmota, were investigated at two sites in the French Alps. The use of a logistic-linear model allowed us to model the probability of marmot settlement in different ecological situations. Marmots preferred sites with a southern or eastern aspect (where snow melts relatively early), intermediate slopes, moderate plant cover, and a low level of human disturbance, and they seemed to select their habitat according to a nested system. To test if habitat quality affected individual fitness, we investigated the effects of sun exposure and two home-range characteristics on litter size at emergence, frequency of female reproduction, and retention of subordinates. Sun exposure and home-range size are two major components of home-range quality that may affect individual fitness.
Canadian Journal of Zoology 02/2011; 72(12):2193-2198. DOI:10.1139/z94-293 · 1.35 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Three main hypotheses have been proposed to explain mate switching in monogamous species: the "better option" hypothesis, the incompatibility hypothesis, and the "forced divorce" hypothesis. We tested the predictions of these hypotheses for the first time in a monogamous mammal using long-term data from a natural population of Alpine marmots (Marmota marmota). Generally, pair disruption resulted in one of the pair members staying on the territory and re-pairing with a younger incomer, whereas the other disappeared from the territory. Replaced individuals were rarely found as dominant in a territory but were often injured or found dead. Individuals gained no benefit from mate switching: new mates were neither heavier, larger, or more heterozygote nor more genetically compatible than previous mates. Moreover, no increase in reproductive success was observed after re-pairing. The relationship between reproductive failure and occurrence of mate change was mainly due to infanticide by the incomer. Our results support the "forced divorce" hypothesis in the Alpine marmot and suggest that mate switching has strong consequences on breeding success. We discuss the importance of taking into account the cases of forced divorce while studying mate switching process and its evolutionary consequences in monogamous species. Copyright 2011, Oxford University Press.
[Show abstract][Hide abstract] ABSTRACT: In human-dominated landscapes, species with large spatial requirements, such as large carnivores, have to deal with human infrastructure and activities within their home ranges. This is the case for the brown bear (Ursus arctos L., 1758) in Scandinavia, which is colonizing more human-dominated landscapes, leading inevitably to an overlap between their home ranges and anthropogenic structures. In this study, we investigated fine-scale habitat selection by brown bears to examine how they deal with this potential disturbance. Using Global Positioning System (GPS) data, we studied (i) habitat selection of female brown bears within their home range and (ii) the influence of diurnal variation in human disturbance on fine-scale habitat use. As expected, females selected habitats within their home range that provided abundant food resources and minimized human-caused disturbance. In addition, our temporal analysis of habitat selection revealed an avoidance of disturbed areas and a selection of slopes by bears during periods of highest human activities, i. e., during daylight hours. We clearly demonstrate the importance of considering the fluctuations in human activity when studying habitat selection, especially at fine spatial scales. Failing to do so may considerably reduce the power to detect important fine-scale habitat-selection behaviors.
Canadian Journal of Zoology 09/2010; 88(9). DOI:10.1139/Z10-053 · 1.35 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: We report the first case of directly observed infanticide in the Alpine marmot (Marmota marmota). Moreover, previous and present observations suggest that 12 young could have been killed by infanticide in the population under study. The bodies of five of them were found with similar neck injuries. In all cases, infanticidal animals were adult males entering a territory in the absence of the resident or having taken over the territory. As in the Arctic ground squirrel, Spermophilus parryii, infanticide could have evolved in Alpine marmots as a part of the reproductive strategy of new resident males. According to ARNOLD (1990), young increase the energetic cost for related animals hibernating with them. Thus, while a rapid return to oestrus is not a realistic outcome, because it occurs only in early spring, infanticide could reduce hibernation costs for the female and increase her reproductive potential in the following year. A sexual selection hypothesis would explain infanticide in Alpine marmot.
Ethology Ecology and Evolution 05/2010; April 1995(2-Vol. 7):191-194. DOI:10.1080/08927014.1995.9522965 · 1.15 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The fitness consequences of heterozygosity and the mechanisms underpinning them are still highly controversial. Using capture-mark-recapture models, we investigated the effects of individual heterozygosity, measured at 16 microsatellite markers, on age-dependent survival and access to dominance in a socially monogamous mammalian species, the alpine marmot. We found a positive correlation between standardized multilocus heterozygosity and juvenile survival. However, there was no correlation between standardized multilocus heterozygosity and either survival of older individuals or access to dominance. The disappearance of a significant heterozygosity fitness correlation when individuals older than juveniles are considered is consistent with the prediction that differences in survival among individuals are maximal early in life. The lack of a correlation between heterozygosity and access to dominance may be a consequence of few homozygous individuals attaining the age at which they might reach dominance. Two hypotheses have been proposed to explain heterozygosity-fitness correlations: genome-wide effects reflected by all markers or local effects of specific markers linked to genes that determine fitness. In accordance with genome-wide effects of heterozygosity, we found significant correlations between heterozygosities calculated across single locus or across two sets of eight loci. Thus, the genome-wide heterozygosity effect seems to explain the observed heterozygosity-fitness correlation in the alpine marmot.
[Show abstract][Hide abstract] ABSTRACT: Using the genetic estimates of paternity available for 22 species of socially monogamous mammals, we investigated the impact of the social structure and of the type of pair bonding on the interspecific variations of extra-pair paternity rates. To this purpose, we classified species in three categories of social structure-solitary, pair or family-living species-and in two categories of pair bonding-intermittent or continuous. We show that interspecific variations of extra-pair paternity rates are better explained by the social structure than by the type of pair bonding. Species with intermittent and continuous pair bonding present similar rates of extra-pair paternity, while solitary and family-living species present higher extra-pair paternity rates than pair-living species. This can be explained by both higher male-male competition and higher female mate choice opportunities in solitary and family-living species than in pair-living species.
[Show abstract][Hide abstract] ABSTRACT: Heterozygosity-fitness correlations (HFCs) are increasingly reported but the underlying mechanisms causing HFCs are generally poorly understood. Here, we test for HFCs in roe deer (Capreolus capreolus) using 22 neutral microsatellites widely distributed in the genome and four microsatellites in genes that are potentially under selection. Juvenile survival was used as a proxy for individual fitness in a population that has been intensively studied for 30 years in northeastern France. For 222 juveniles, we computed two measures of genetic diversity: individual heterozygosity (H), and mean d(2) (relatedness of parental genomes). We found a relationship between genetic diversity and fitness both for the 22 neutral markers and two candidate genes: IGF1 (Insulin-like Growth Factor I) and NRAMP (natural resistance-associated macrophage protein). Statistical evidence and the size of genetic effects on juvenile survival were comparable to those reported for early development and cohort variation, suggesting a substantial influence of genetic components on fitness in this roe deer population. For the 22 neutral microsatellites, a correlation with fitness was revealed for mean d(2), but not for H, suggesting a possible outbreeding advantage. This heterosis effect could have been favored by introduction of genetically distant (Hungarian) roe deer to the population in recent times and, possibly, by the structuring of the population into distinct clans. The locus-specific correlations with fitness may be driven by growth rate advantages and resistance to diseases known to exist in the studied population. Our analyses of neutral and candidate gene markers both suggest that the observed HFCs are likely mainly due to linkage with dominant or overdominant loci that affect fitness ("local" effect) rather than to a genome-wide relationship with homozygosity due to inbreeding ("general" effect).
[Show abstract][Hide abstract] ABSTRACT: Extrapair paternity is widespread in birds and mammals. In particular, the alpine marmot, Marmota marmota, has a high frequency of extrapair paternity that seems to be explained by the genetic compatibility hypothesis. We investigated whether the number and proportion of extrapair young depend on the heterozygosity (individual genetic diversity) of the social male, or on the genetic similarity between the social male and his mate (relatedness). Both the number and the proportion of extrapair young increased with both high similarity and dissimilarity between the social pair. In combination with previous results, our study suggests that patterns of extrapair paternity in alpine marmots can best be explained by the genetic compatibility hypothesis, and more precisely its optimal outbreeding variant. Our results indeed suggest that extrapair paternity is a mechanism to avoid both in- and outbreeding depression. We discuss which proximal mechanisms may be involved in extrapair paternity in this species.
[Show abstract][Hide abstract] ABSTRACT: The aim of this study is to empirically illustrate the importance of taking movement constraints into account when testing for habitat selection with telemetry data. Global Positioning System relocations of two Scandinavian brown bears were used to compare the results of two different tests of habitat selection by the bears within their home range. Both relied on the comparison of observed dataset with datasets simulated under the hypothesis of random habitat use. The first analysis did not take movement constraints into account (simulations were carried out by randomly distributing a set of points in the home range) whereas the second analysis accounted for these constraints (simulations were carried out by building random trajectories in the home range). The results for the two analyses showed contrasted results. Therefore, not accounting for movement constraints in analyses may result in a misleading biological interpretation. Autocorrelation between relocations is not undesirable: it contains information about ecological processes that should be integrated in habitat selection analyses.