Senescence or selective disappearance? Age trajectories of body mass in wild and captive populations of a small-bodied primate.

Classic theories of ageing consider extrinsic mortality (EM) a major factor in shaping longevity and ageing, yet most studies of functional ageing focus on species with low EM. This bias may cause overestimation of the influence of senescent declines in performance over condition-dependent mortality on demographic processes across taxa. To simultaneously investigate the roles of functional senescence (FS) and intrinsic, extrinsic and condition-dependent mortality in a species with a high predation risk in nature, we compared age trajectories of body mass (BM) in wild and captive grey mouse lemurs (Microcebus murinus) using longitudinal data (853 individuals followed through adulthood). We found evidence of non-random mortality in both settings. In captivity, the oldest animals showed senescence in their ability to regain lost BM, whereas no evidence of FS was found in the wild. Overall, captive animals lived longer, but a reversed sex bias in lifespan was observed between wild and captive populations. We suggest that even moderately condition-dependent EM may lead to negligible FS in the wild. While high EM may act to reduce the average lifespan, this evolutionary process may be counteracted by the increased fitness of the long-lived, high-quality individuals.

A novel system of polymorphic and diverse NK cell receptors in primates.

There are two main classes of natural killer (NK) cell receptors in mammals, the killer cell immunoglobulin-like receptors (KIR) and the structurally unrelated killer cell lectin-like receptors (KLR). While KIR represent the most diverse group of NK receptors in all primates studied to date, including humans, apes, and Old and New World monkeys, KLR represent the functional equivalent in rodents. Here, we report a first digression from this rule in lemurs, where the KLR (CD94/NKG2) rather than KIR constitute the most diverse group of NK cell receptors. We demonstrate that natural selection contributed to such diversification in lemurs and particularly targeted KLR residues interacting with the peptide presented by MHC class I ligands. We further show that lemurs lack a strict ortholog or functional equivalent of MHC-E, the ligands of non-polymorphic KLR in "higher" primates. Our data support the existence of a hitherto unknown system of polymorphic and diverse NK cell receptors in primates and of combinatorial diversity as a novel mechanism to increase NK cell receptor repertoire.

Compatibility counts: MHC-associated mate choice in a wild promiscuous primate.

The mechanisms and temporal aspects of mate choice according to genetic constitution are still puzzling. Recent studies indicate that fitness is positively related to diversity in immune genes (MHC). Both sexes should therefore choose mates of high genetic quality and/or compatibility. However, studies addressing the role of MHC diversity in pre- and post-copulatory mate choice decisions in wild-living animals are few. We investigated the impact of MHC constitution and of neutral microsatellite variability on pre- and post-copulatory mate choice in both sexes in a wild population of a promiscuous primate, the grey mouse lemur (Microcebus murinus). There was no support for pre-copulatory male or female mate choice, but our data indicate post-copulatory mate choice that is associated with genetic constitution. Fathers had a higher number of MHC supertypes different from those of the mother than randomly assigned males. Fathers also had a higher amino acid distance to the females' MHC as well as a higher total number of MHC supertypes and a higher degree of microsatellite heterozygosity than randomly assigned males. Female cryptic choice may be the underlying mechanism that operates towards an optimization of the genetic constitution of offspring. This is the first study that provides support for the importance of the MHC constitution in post-copulatory mate choice in non-human primates.

The costs of risky male behaviour: sex differences in seasonal survival in a small sexually monomorphic primate.

Male excess mortality is widespread among mammals and frequently interpreted as a cost of sexually selected traits that enhance male reproductive success. Sex differences in the propensity to engage in risky behaviours are often invoked to explain the sex gap in survival. Here, we aim to isolate and quantify the survival consequences of two potentially risky male behavioural strategies in a small sexually monomorphic primate, the grey mouse lemur Microcebus murinus: (i) most females hibernate during a large part of the austral winter, whereas most males remain active and (ii) during the brief annual mating season males roam widely in search of receptive females. Using a 10-year capture-mark-recapture dataset from a population of M. murinus in Kirindy Forest, western Madagascar, we statistically modelled sex-specific seasonal survival probabilities. Surprisingly, we did not find any evidence for direct survival benefits of hibernation-winter survival did not differ between males and females. By contrast, during the breeding season males survived less well than females (sex gap: 16%). Consistent with the 'risky male behaviour' hypothesis, the period for lowered male survival was restricted to the short mating season. Thus, sex differences in survival in a promiscuous mammal can be substantial even in the absence of sexual dimorphism.

Walk the line-dispersal movements of gray mouse lemurs (Microcebus murinus).

Despite the importance of dispersal for individuals and populations, little is known about the actual dispersal process in most species. We observed 90 subadult gray mouse lemurs-small, arboreal, nocturnal primates-in Kirindy Forest in western Madagascar, to determine the behavioral processes underlying natal dispersal. Twelve radio-collared males dispersed over distances between 180 and 960 m (≈1-7 home range diameters) away from their presumed natal ranges. Dispersal forays were fast and highly directed, and thus distinct from routine movements. Contrary to expectations of current hypotheses on potential differences between different types of dispersal movements, their special movement style did not prevent dispersers from interrupting forays to exploit resources they encountered during their forays. Data from a translocation experiment indicated that highly directed dispersal or search forays reflect a general strategy for large-scale exploration away from familiar sites in this species. A prolonged transfer phase was also observed, with regular commuting between old and new sites for up to 14 days, which probably served to moderate costs of unfamiliarity with a new site. In conclusion, the dispersal process of gray mouse lemurs is characterized by high intra- and interindividual consistency in movement strategies, but variation in the duration of the transfer phase. The observed dispersal movement style represents an effective strategy balancing costs of dispersal with the need to gather an appropriate level of information about potential dispersal target sites. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1007/s00265-012-1371-y) contains supplementary material, which is available to authorized users.

Functional associations of similar MHC alleles and shared parasite species in two sympatric lemurs.

Several recent studies of animals in their natural surroundings found evidence for effects of certain major histocompatibility complex (MHC) immune gene alleles on the parasite load. However, in multi-infected individuals the particular selection pressure exerted by specific parasites has rarely been explored. In this study we took advantage of the parasitological and genetic data of two previously investigated Malagasy lemur species (Cheirogaleus medius and Microcebus murinus). We investigated whether the two sympatric and ecologically similar primates are infected by similar parasite species and explored if certain parasites are associated with particular MHC alleles. Our study revealed that most of the parasite egg morphotypes were found in both hosts. In each lemur species we identified one MHC allele which was positively associated with Ascaris-infection. Interestingly, these MHC alleles were very similar to each other but differed from all other investigated MHC alleles in an amino acid substitution in a putative functional important antigen binding site. Thus, our study gives first intriguing evidence for a direct connection between certain antigen binding sites of MHC molecules with a particular parasite in two wild primate populations. This may indicate that indeed certain parasites exert direct selective pressure on the MHC of wild living hosts.

Mutualism, reciprocity, or kin selection? Cooperative rescue of a conspecific from a boa in a nocturnal solitary forager the gray mouse lemur.

Predator mobbing is a widespread phenomenon in many taxa but the evolution of cooperative mobbing as an adaptive behavior is still subject to debate. Here, we report evidence for cooperative predator defense in a nocturnal solitarily foraging primate, the gray mouse lemur (Microcebus murinus). Several mouse lemurs mobbed a snake that held a non-related male conspecific until he could escape. Evolutionary hypotheses to explain cooperative mobbing include (1) by-product mutualism, when individuals defend others in the process of defending themselves; (2) reciprocity, where animals achieve a higher fitness when helping each other than when they do not cooperate; and (3) kin selection where animals help each other only if they share genes by common descent. Owing to the solitary activity of this species, reciprocity seems to be least likely to explain our observations. By-product mutualism cannot be ruled out entirely but, if costs of snake mobbing are relatively low, the available detailed socio-genetic information indicates that kin selection, rather than any of the other proposed mechanisms, is the primary evolutionary force behind the observed cooperative rescue.