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Concept: Mouse lemur

178

BACKGROUND: Kin selection is a driving force in the evolution of mammalian social complexity. Recognition of paternal kin using vocalizations occurs in taxa with cohesive, complex social groups. This is the first investigation of paternal kin recognition via vocalizations in a small-brained, solitary foraging mammal, the grey mouse lemur (Microcebus murinus), a frequent model for ancestral primates. We analyzed the high frequency/ultrasonic male advertisement (courtship) call and alarm call. RESULTS: Multi-parametric analyses of the calls' acoustic parameters and discriminant function analyses showed that advertisement calls, but not alarm calls, contain patrilineal signatures. Playback experiments controlling for familiarity showed that females paid more attention to advertisement calls from unrelated males than from their fathers. Reactions to alarm calls from unrelated males and fathers did not differ. CONCLUSIONS: 1) Findings provide the first evidence of paternal kin recognition via vocalizations in a small-brained, solitarily foraging mammal. 2) High predation, small body size, and dispersed social systems may select for acoustic paternal kin recognition in the high frequency/ultrasonic ranges, thus limiting risks of inbreeding and eavesdropping by predators or conspecific competitors. 3) Paternal kin recognition via vocalizations in mammals is not dependent upon a large brain and high social complexity, but may already have been an integral part of the dispersed social networks from which more complex, kin-based sociality emerged.

Concepts: Selection, Mammal, Human, Primate, Mouse lemur, Gray Mouse Lemur

168

BACKGROUND: Hematologic and biochemical data are needed to characterize the health status of animal populations over time to determine the habitat quality and captivity conditions. Blood components and the chemical entities that they transport change predominantly with sex and age. The aim of this study was to utilize blood chemistry monitoring to establish the reference levels in a small prosimian primate, the Grey Mouse Lemur (Microcebus murinus). METHOD: In the captive colony, mouse lemurs may live 10-12 years, and three age groups for both males and females were studied: young (1-3 years), middle-aged (4-5 years) and old (6-10 years). Blood biochemical markers were measured using the VetScan Comprehensive Diagnostic Profile. Because many life history traits of this primate are highly dependent on the photoperiod (body mass and reproduction), the effect of season was also assessed. RESULTS: The main effect of age was observed in blood markers of renal functions such as creatinine, which was higher among females. Additionally, blood urea nitrogen significantly increased with age and is potentially linked to chronic renal insufficiency, which has been described in captive mouse lemurs. The results demonstrated significant effects related to season, especially in blood protein levels and glucose rates; these effects were observed regardless of gender or age and were likely due to seasonal variations in food intake, which is very marked in this species. CONCLUSION: These results were highly similar with those obtained in other primate species and can serve as references for future research of the Grey Mouse Lemur.

Concepts: Prosimian, Cheirogaleidae, Primate, Renal failure, Gray Mouse Lemur, Lemur, Mouse lemur

25

Glucocorticoid hormones are known to play a key role in mediating a cascade of physiological responses to social and ecological stressors and can therefore influence animals' behaviour and ultimately fitness. Yet, how glucocorticoid levels are associated with reproductive success or survival in a natural setting has received little empirical attention so far. Here, we examined links between survival and levels of glucocorticoid in a small, short-lived primate, the grey mouse lemur (Microcebus murinus), using for the first time an indicator of long-term stress load (hair cortisol concentration). Using a capture-mark-recapture modelling approach, we assessed the effect of stress on survival in a broad context (semi-annual rates), but also under a specific period of high energetic demands during the reproductive season. We further assessed the power of other commonly used health indicators (body condition and parasitism) in predicting survival outcomes relative to the effect of long-term stress.

Concepts: Lemur, Cheirogaleidae, Gray Mouse Lemur, Mouse lemur

15

Mouse lemurs are basal primates that rely on chemo- and acoustic signalling for social interactions in their dispersed social systems. We examined the urinary protein content of two mouse lemurs species, within and outside the breeding season, to assess candidates used in species discrimination, reproductive or competitive communication. Urine from Microcebus murinus and Microcebus lehilahytsara contain a predominant 10 kDa protein, expressed in both species by some, but not all, males during the breeding season, but at very low levels by females. Mass spectrometry of the intact proteins confirmed the protein mass and revealed a 30 Da mass difference between proteins from the two species. Tandem mass spectrometry after digestion with three proteases and sequencing de novo defined the complete protein sequence and located an Ala/Thr difference between the two species that explained the 30 Da mass difference. The protein (mature form: 87 amino acids) is an atypical member of the whey acidic protein family (WFDC12). Seasonal excretion of this protein, species difference and male-specific expression during the breeding season suggest that it may have a function in intra- and/or intersexual chemical signalling in the context of reproduction, and could be a cue for sexual selection and species recognition.

Concepts: Proteins, Gene, Acid, Amino acid, Reproduction, Mass spectrometry, Mouse lemur, Protein

12

Implementation of the coalescent model in a Bayesian framework is an emerging strength in genetically-based species delimitation studies. By providing an objective measure of species diagnosis, these methods represent a quantitative enhancement to the analysis of multi-locus data, and complement more traditional methods based on phenotypic and ecological characteristics. Recognized as two species 20 years ago, mouse lemurs (genus Microcebus) now comprise more than 20 species, largely diagnosed from mtDNA sequence data. With each new species description, enthusiasm has been tempered with scientific skepticism. Here, we present a statistically justified and unbiased Bayesian approach towards mouse lemur species delimitation. We perform validation tests using multi-locus sequence data and two methodologies: (1) reverse-jump Markov chain Monte Carlo sampling to assess the likelihood of different models defined a priori by a guide tree, and (2) a Bayes factor delimitation test that compares different species-tree models without a guide tree. We assess the sensitivity of these methods using randomized individual assignments, which has been used in BPP studies, but not with Bayes factor delimitation tests. Our results validate previously diagnosed taxa, as well as new species hypotheses, resulting in support for three new mouse lemur species. As the challenge of multiple researchers using differing criteria to describe diversity is not unique to Microcebus, the methods used here have significant potential for clarifying diversity in other taxonomic groups. We echo Carstens et al. (2013) in advocating that multiple lines of evidence, including use of the coalescent model, should be trusted to delimit new species. This article is protected by copyright. All rights reserved.

Concepts: Bayesian statistics, Monte Carlo, Likelihood function, Markov chain Monte Carlo, Scientific method, Mouse lemur, Lemur, Bayesian inference

5

Phylogeographic analysis can be described as the study of the geological and climatological processes that have produced contemporary geographic distributions of populations and species. Here, we attempt to understand how the dynamic process of landscape change on Madagascar has shaped the distribution of a targeted clade of mouse lemurs (genus Microcebus) and, conversely, how phylogenetic and population genetic patterns in these small primates can reciprocally advance our understanding of Madagascar’s prehuman environment. The degree to which human activity has impacted the natural plant communities of Madagascar is of critical and enduring interest. Today, the eastern rainforests are separated from the dry deciduous forests of the west by a large expanse of presumed anthropogenic grassland savanna, dominated by the Family Poaceae, that blankets most of the Central Highlands. Although there is firm consensus that anthropogenic activities have transformed the original vegetation through agricultural and pastoral practices, the degree to which closed-canopy forest extended from the east to the west remains debated. Phylogenetic and population genetic patterns in a five-species clade of mouse lemurs suggest that longitudinal dispersal across the island was readily achieved throughout the Pleistocene, apparently ending at ∼55 ka. By examining patterns of both inter- and intraspecific genetic diversity in mouse lemur species found in the eastern, western, and Central Highland zones, we conclude that the natural environment of the Central Highlands would have been mosaic, consisting of a matrix of wooded savanna that formed a transitional zone between the extremes of humid eastern and dry western forest types.

Concepts: Species, Ecosystem, Savanna, Primate, Mouse lemur, Forest, Biology, Lemur

4

Among anthropogenic pressures, light pollution altering light/dark cycles and changing the nocturnal component of the environment constitutes a threat for biodiversity. Light pollution is widely spread across the world and continuously growing. However, despite the efforts realized to describe and understand the effects of artificial lighting on fauna, few studies have documented its consequences on biological rhythms, behavioral and physiological functions in nocturnal mammals. To determine the impacts of light pollution on nocturnal mammals an experimental study was conducted on a nocturnal primate, the grey mouse lemur Microcebus murinus. Male mouse lemurs (N = 8) were exposed 14 nights to moonlight treatment and then exposed 14 nights to light pollution treatment. For both treatments, chronobiological parameters related to locomotor activity and core temperature were recorded using telemetric transmitters. In addition, at the end of each treatment, the 14(th) night, nocturnal and feeding behaviors were explored using an infrared camera. Finally, throughout the study, body mass and daily caloric food intake were recorded. For the first time in a nocturnal primate, light pollution was demonstrated to modify daily rhythms of locomotor activity and core temperature especially through phase delays and increases in core temperature. Moreover, nocturnal activity and feeding behaviors patterns were modified negatively. This study suggests that light pollution induces daily desynchronization of biological rhythms and could lead to seasonal desynchronization with potential deleterious consequences for animals in terms of adaptation and anticipation of environmental changes.

Concepts: Primate, Lemur, Gray Mouse Lemur, Mouse lemur

3

Longitudinal sampling for intestinal microbiota in wild animals is difficult, leading to a lack of information on bacterial dynamics occurring in nature. We studied how the composition of microbiota communities changed temporally in free-ranging small primates, rufous mouse lemurs (Microcebus rufus). We marked and recaptured mouse lemurs during their mating season in Ranomafana National Park in southeastern mountainous rainforests of Madagascar for two years and determined fecal microbiota of these mouse lemurs with MiSeq sequencing. We collected 160 fecal samples from 71 animals and had two or more samples from 39 individuals. We found small, but statistically significant, effects of site and age in microbiota richness and diversity, and sex, year and site in microbiota composition, whilst the within-year temporal trends were less clear. Within-host microbiota showed pervasive variation in intestinal bacterial community composition, especially during the second study year. We hypothesize that the biological properties of mouse lemurs, including, small body size and fast metabolism may contribute to the temporal intra-individual level variation, something that should be testable with more extensive sampling regimes.

Concepts: Cheirogaleidae, Evolution, Metabolism, Gut flora, Mouse lemur, Bacteria, Lemur, Primate

3

Increasingly, individual variation in personality has become a focus of behavioral research in animal systems. Boldness and shyness, often quantified as the tendency to explore novel situations, are seen as personality traits important to the fitness landscape of individuals. Here we tested for individual differences within and across contexts in behavioral responses of captive mouse lemurs (Microcebus murinus) to novel objects, novel foods, and handling. We report consistent differences in behavioral responses for objects and handling. We also found that the responses to handling and novel objects were correlated and repeatable. Lastly, we show that shyer individuals may show less variability in their behavioral responses. This study provides new information on the potential for behavioral syndromes in this species and highlights differences in the degree to which behavioral types (e.g., shy/bold) vary in their behavioral responses.

Concepts: Avoidant personality disorder, Lemur, Gray Mouse Lemur, Person, Psychology, Boldness, Mouse lemur, Shyness

2

Age-associated cognitive impairment is a major health and social issue because of increasing aged population. Cognitive decline is not homogeneous in humans and the determinants leading to differences between subjects are not fully understood. In middle-aged healthy humans, fasting blood glucose levels in the upper normal range are associated with memory impairment and cerebral atrophy. Due to a close evolutional similarity to Man, non-human primates may be useful to investigate the relationships between glucose homeostasis, cognitive deficits and structural brain alterations. In the grey mouse lemur, Microcebus murinus, spatial memory deficits have been associated with age and cerebral atrophy but the origin of these alterations have not been clearly identified. Herein, we showed that, on 28 female grey mouse lemurs (age range 2.4-6.1 years-old), age correlated with impaired fasting blood glucose (rs=0.37) but not with impaired glucose tolerance or insulin resistance. In middle-aged animals (4.1-6.1 years-old), fasting blood glucose was inversely and closely linked with spatial memory performance (rs=0.56) and hippocampus (rs=-0.62) or septum (rs=-0.55) volumes. These findings corroborate observations in humans and further support the grey mouse lemur as a natural model to unravel mechanisms which link impaired glucose homeostasis, brain atrophy and cognitive processes.

Concepts: Brain, Cheirogaleidae, Cognition, Gray Mouse Lemur, Primate, Blood sugar, Lemur, Mouse lemur