Mate choice for neutral and MHC genetic characteristics in Alpine marmots : different targets in different contexts?

We warmly thank all students and Earthwatch volunteers involved in catching the marmots and the authorities of the Vanoise National Park for granting us permission to work in the Grande Sassière Nature Reserve. We thank M. Harrington for English editing and Dr. E. Rajon for helpful discussions on the manuscript. This work was supported by the "Agence Nationale de la Recherche" (ANR, project ANR-08-BLAN-0214-03, ANR-13-JSV7-0005), the "Centre National de la Recherche Scientifique" (CNRS), the "FR41 BioEnvironnement et Santé de l'Université de Lyon" and the "Earthwatch Institute", the scholarship for postgraduate studies "Obra Social Fundació La Caixa" and Vetagro-Sup.Sexual selection through female mate choice for genetic characteristics has been suggested to be an important evolutionary force maintaining genetic variation in animal populations. However, the genetic targets of female mate choice are not clearly identified and whether female mate choice is based on neutral genetic characteristics or on particular functional loci remains an open question. Here, we investigated the genetic targets of female mate choice in Alpine marmots (Marmota marmota), a socially monogamous mammal where extra-pair paternity (EPP) occurs. We used 16 microsatellites to describe neutral genetic characteristics and two MHC loci belonging to MHC class I and II as functional genetic characteristics. Our results reveal that (1) neutral and MHC genetic characteristics convey different information in this species, (2) social pairs show a higher MHC class II dissimilarity than expected under random mate choice, and (3) the occurrence of EPP increases when social pairs present a high neutral genetic similarity or dissimilarity but also when they present low MHC class II dissimilarity. Thus, female mate choice is based on both neutral and MHC genetic characteristics, and the genetic characteristics targeted seem to be context dependent (i.e., the genes involved in social mate choice and genetic mate choice differ). We emphasize the need for empirical studies of mate choice in the wild using both neutral and MHC genetic characteristics because whether neutral and functional genetic characteristics convey similar information is not universal

Technical validation and a comparison of two methods to quantify individual levels of glucocorticoids in Alpine marmot hair

Quantification of cortisol concentration in hair has become a promising conservation tool for non-invasive monitoring of “stress” in wild populations, yet this method needs to be carefully validated for each species. The goals of the study were: • Immunologically validate two methods (study 1 and 2 respectively) to extract and quantify cortisol in the hair of wild Alpine marmots. • Compare the amount of cortisol extracted from hair samples using two methods i.e. cut into fine pieces (study 1) and hair samples pulverized using a ball mill (study 2). • Determine the extent to which methods in study 2 could provide individual specific hair cortisol (HC) measures when samples were taken from the same body location. Within and between individual variations in HC levels were examined from multiple hair samples from 14 subjects in study 2. We evaluated if inter-individual variations in HC levels could be explained by sex and age. At least twice the amount of cortisol was obtained per g/hair when samples were pulverized in a ball mill prior to extraction compared to when cut into pieces. Our methods demonstrated intra-individual consistency in HC at a given time point: inter-individual variation in HC was three times larger than within individual variance. Sex and age did not impact HC levels

Early and Adult Social Environments Shape Sex-Specific Actuarial Senescence Patterns in a Cooperative Breeder

Sociality modulates life-history traits through changes in resource allocation to fitness-related traits. However, how social factors at different stages of the life cycle modulate senescence remains poorly understood. To address this question, we assessed the influence of social environment in both early life and adulthood on actuarial senescence in the Alpine marmot, a cooperative breeder. The influence of helpers on actuarial senescence strongly differed depending on when help was provided and on the sex of the dominant. Being helped when adult slowed down senescence in both sexes. However, the effect of the presence of helpers during the year of birth of a dominant was sex specific. Among dominants helped during adulthood, females born in the presence of helpers senesced slower, whereas males senesced faster. Among dominants without helpers during adulthood, females with helpers at birth senesced faster. Social environment modulates senescence but acts differently between sexes and life stages

Sex differences in adult lifespan and aging rates of mortality across wild mammals

International audienc

Paternity and Dominance Loss in Male Breeders: The Cost of Helpers in a Cooperatively Breeding Mammal

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

Ice-Age Climate Adaptations Trap the Alpine Marmot in a State of Low Genetic Diversity.

Some species responded successfully to prehistoric changes in climate [1, 2], while others failed to adapt and became extinct [3]. The factors that determine successful climate adaptation remain poorly understood. We constructed a reference genome and studied physiological adaptations in the Alpine marmot (Marmota marmota), a large ground-dwelling squirrel exquisitely adapted to the "ice-age" climate of the Pleistocene steppe [4, 5]. Since the disappearance of this habitat, the rodent persists in large numbers in the high-altitude Alpine meadow [6, 7]. Genome and metabolome showed evidence of adaptation consistent with cold climate, affecting white adipose tissue. Conversely, however, we found that the Alpine marmot has levels of genetic variation that are among the lowest for mammals, such that deleterious mutations are less effectively purged. Our data rule out typical explanations for low diversity, such as high levels of consanguineous mating, or a very recent bottleneck. Instead, ancient demographic reconstruction revealed that genetic diversity was lost during the climate shifts of the Pleistocene and has not recovered, despite the current high population size. We attribute this slow recovery to the marmot's adaptive life history. The case of the Alpine marmot reveals a complicated relationship between climatic changes, genetic diversity, and conservation status. It shows that species of extremely low genetic diversity can be very successful and persist over thousands of years, but also that climate-adapted life history can trap a species in a persistent state of low genetic diversity.This work was supported by the Francis Crick Institute which receives its core funding from Cancer Research UK (FC001134), the UK Medical Research Council (FC001134), and the Wellcome Trust (FC001134). CB and AC are supported by the Agence Nationale de la Recherche (project ANR-13-JSV7-0005) and the Centre National de la Recherche Scientifique (CNRS), CB is supported by the Rhône-Alpes region (Grant 15.005146.01). LD is supported by Agence Nationale de la Recherche (project ANR-12-ADAP-0009). TIG is supported by a Leverhulme Early Career Fellowship (Grant ECF-2015-453) and a NERC grant (NE/N013832/1). JMG is supported by a Hertha Finberg Fellowship (FWF T703). LDR is supported by the Diabetes UK RD Lawrence Fellowship (16/0005382)

avpr-1a lengths of Alpine marmot females and extra-pair behaviour

Female avpr-1a lengths, extra-pair paternity occurence, social pair genetic relatedness and presence-absence of male subordinate

Annual proportion of extra-pair litters

Annual proportion of extra-pair litters, annual climatic variables and annual proportion of families with sexually mature male subordinate