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Investigating factors influencing infant physical and social development is important to elucidate primate adaptations and life history evolution. Infant sifakas exhibit a puzzling mismatch between dental precocity and relatively slow postnatal growth, but only anecdotal reports of infant development are available for a comparative appraisal of their early life history and maturation. We therefore collected behavioral data on mother–infant dyads of 16 infant Verreaux’s sifakas (Propithecus verreauxi) from 3 birth cohorts in Kirindy Forest to assess how the infant’s age, sex, mother’s age, and environmental variation influence the infant’s development until weaning. We found that somatic growth rates differed between the sexes, with females growing faster than males. Infants began ingesting solid food as early as 3 weeks of age, which is extremely early for a primate of this size and much earlier than in Lemuridae. Social behavior emerged at a later age than motor skills. Despite pronounced variation in the timing and occurrence of various infant activities, none of them differed between the sexes, except that male infants were more engaged in grooming others than females. Infant sifakas did not develop faster than other lemurs despite the extra available energy gained from ingesting solid food at an early age, but their mothers carry them for a relatively long period, perhaps because vertical clinging and leaping is a locomotor style that requires prolonged physical maturation. The adaptive significance of their dental precocity remains elusive, however. Thus, further studies are required to understand how developmental schedules have coevolved with ecological and anatomical factors.

The cestode Hymenolepis nana is a common parasite of humans and mice. Fecal shedding in the absence of clinical disease has previously been reported in ring-tailed lemurs ( Lemur catta). This report describes fatal, disseminated H. nana cestodiasis infection in an aged ring-tailed lemur in a zoological collection. The parasites were associated with severe multifocal to coalescing and regionally extensive pyogranulomatous hepatitis and moderate multifocal pneumonia. The morphology of the parasites was highly unusual. Profiles were variably sized, ellipsoid to irregularly serpiginous, lined by a thin tegument, and filled with lightly eosinophilic fibrillar stroma and numerous, round basophilic cells. Polymerase chain reaction targeting a portion of the 18S rRNA gene and DNA sequencing of the amplicon showed 100% homology with H. nana. Esther E. V. Crouch et al, Fatal Hymenolepis nana cestodiasis in a ring-tailed lemur (Lemur catta), Veterinary Pathology (, ) pp. . Copyright © 2021. DOI: 10.1177/03009858211042580. Users who receive access to an article through a repository are reminded that the article is protected by copyright and reuse is restricted to non-commercial and no derivative uses. Users may also download and save a local copy of an article accessed in an institutional repository for the user's personal reference. For permission to reuse an article, please follow our Process for Requesting Permission. Deposited by shareyourpaper.org and openaccessbutton.org. We've taken reasonable steps to ensure this content doesn't violate copyright. However, if you think it does you can request a takedown by emailing help@openaccessbutton.org.

Infanticide occurs in an array of mammalian species, especially primates. Most infanticidal events occur in polygynous societies, though they sometimes happen in nongregarious populations. We witnessed a possible infanticidal event of a 3-month-old male aye-aye, a species that exhibits a dispersed multimale social system, in Torotorofotsy, Madagascar. Though firsthand killing of the infant was not observed, physical injuries to the infant, vocalizations of the adult female, and her subsequent chase of the adult male aye-aye strongly indicates infanticide. If true, this would be the first recorded incident of an infanticidal event in a noyau primate. The evidence for three different explanations of infanticide is evaluated.

Portraits of humans favour the left cheek, with emotion thought to drive this posing asymmetry. In primates the emotion-dominant right hemisphere predominantly controls the left hemiface, rendering the left cheek anatomically more expressive than the right. As perceptions of nonhuman primates vary with genetic relatedness, depictions of nonhuman primates should theoretically be influenced by their phylogenetic proximity to humans. The present study thus examined whether humans depict nonhuman primates showing the left cheek, and whether depictions vary with evolutionary distance. Photographs of nonhuman primates were sourced from Instagram's "Most recent" feed: great apes (#chimpanzee, #bonobo, #gorilla, #orangutan), lesser apes (#gibbon), Old World monkeys (#baboon, #macaque, #proboscismonkey), New World monkeys (#spidermonkey, #marmosetmonkey, #capuchin), and prosimians (#lemur, #slowloris, #tarsier). The first 500 single-subject images for each hashtag (except #slowloris for which 318 images were available) were coded for pose orientation (left, right) and portrait type (head/torso, full body). As anticipated, there was a left cheek bias for great apes but no bias for more distantly related primates. These data thus suggest that depictions of nonhuman primates are implicitly influenced by phylogenetic proximity: the more closely related the primate, the more likely we are to depict them as we do ourselves, showing the left cheek.

In recent years, interest in understanding the effects of climate change on species and ecological systems has sharply increased. We quantify and contextualize the current state of knowledge about the effects of contemporary climate change on non-human primates, a taxon of great ecological and anthropological significance. Specifically, we report findings from a systematic literature search designed to assess the allocation of research effort on primates and climate change and consider how the current distribution of knowledge may be influencing our understanding of the topic. We reveal significant phylogenetic and geographic gaps in our knowledge, which is strongly biased towards lemurs, apes, and a relatively small subset of primate range countries. We show that few analyses investigate changes in primate foods relative to changes in primates themselves or their habitats, and observe that few longitudinal datasets are of sufficient duration to detect effects on the generational scale. We end by identifying areas of research inquiry that would advance our theoretical understanding of primate ecology, evolution, and adaptability, and meaningfully contribute to primate conservation.

Contains fulltext : 237107.pdf (Publisher’s version ) (Open Access) Comparative neuroimaging has been used to identify changes in white matter architecture across primate species phylogenetically close to humans, but few have compared the phylogenetically distant species. Here, we acquired postmortem diffusion imaging data from ring-tailed lemurs (Lemur catta), black-capped squirrel monkeys (Saimiri boliviensis), and rhesus macaques (Macaca mulatta). We were able to establish templates and surfaces allowing us to investigate sulcal, cortical, and white matter anatomy. The results demonstrate an expansion of the frontal projections of the superior longitudinal fasciculus complex in squirrel monkeys and rhesus macaques compared to ring-tailed lemurs, which correlates with sulcal anatomy and the lemur's smaller prefrontal granular cortex. The connectivity of the ventral pathway in the parietal region is also comparatively reduced in ring-tailed lemurs, with the posterior projections of the inferior longitudinal fasciculus not extending toward parietal cortical areas as in the other species. In the squirrel monkeys we note a very specific occipito-parietal anatomy that is apparent in their surface anatomy and the expansion of the posterior projections of the optical radiation. Our study supports the hypothesis that the connectivity of the prefrontal-parietal regions became relatively elaborated in the simian lineage after divergence from the prosimian lineage. 17 p.

Background: The ring-tailed lemur (Lemur catta) is a charismatic strepsirrhine primate endemic to Madagascar. These lemurs are of particular interest, given their status as a flagship species and widespread publicity in the popular media. Unfortunately, a recent population decline has resulted in the census population decreasing to, The project that gave rise to these results received the support of 2 fellowships from "la Caixa" Foundation (ID 100010434) and from the European Union's Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement No. 847648. The fellowship codes are LCF/BQ/PI20/11760004 and LCF/BQ/DR20/11790032. T.M.B. is supported by funding from the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation programme (grant agreement No. 864203), BFU2017-86471-P (MINECO/FEDER, UE), “Unidad de Excelencia María de Maeztu,” funded by the AEI (CEX2018-000792-M), Howard Hughes International Early Career, NIH 1R01HG010898-01A1, and Secretaria d'Universitats i Recerca and CERCA Programme del Departament d'Economia i Coneixement de la Generalitat de Catalunya (GRC 2017 SGR 880).

Inference by exclusion, or the ability to select a correct course of action by systematically excluding other potential alternatives, is a form of logical inference that allows individuals to solve problems without complete information. Current comparative research shows that several bird, mammal and primate species can find hidden food through inference by exclusion. Yet there is also wide variation in how successful different species are as well as the kinds of sensory information they can use to do so. An important question is therefore why some species are better at engaging in logical inference than others. Here, we investigate the evolution of logical reasoning abilities by comparing strepsirrhine primate species that vary in dietary ecology: frugivorous ruffed lemurs (Varecia spp.) and folivorous Coquerel's sifakas, Propithecus coquereli. Across two studies, we examined their abilities to locate food using direct information versus inference from exclusion and using both visual and auditory information. In study 1, we assessed whether these lemurs could make inferences when full visual and auditory information about the two potential locations of food were provided. In study 2, we then compared their ability to make direct inferences versus inferences by exclusion in both the visual and auditory domains. We found that these lemur species can use visual information to find food, but that only ruffed lemurs were also able to use auditory cues, mirroring differences in the complexity of their wild ecology. We further found that, unlike many anthropoid species tested to date, these strepsirrhine species failed to make inferences by exclusion. These results highlight the importance of natural history in understanding the evolution of logical inference and help reconstruct the deeper phylogeny of primate cognition.

Objectives Variation in primate masticatory form and function has been extensively researched through both morphological and experimental studies. As a result, symphyseal fusion in different primate clades has been linked to either the recruitment of vertically directed balancing-side muscle force, the timing and recruitment of transversely directed forces, or both. This study investigates the relationship between jaw muscle activity patterns and morphology in extant primates to make inferences about masticatory function in extinct primates, with implications for understanding the evolution of symphyseal fusion. Materials and methods Three-dimensional mandibular landmark data were collected for 31 extant primates and nine fossil anthropoids and subfossil lemur species. Published electromyography (EMG) data were available for nine of the extant primate species. Partial least squares analysis and phylogenetic partial least squares analysis were used to identify relationships between EMG and jaw shape data and evaluate variation in jaw morphology. Results Primates with partial and complete symphyseal fusion exhibit shape-function patterns associated with the wishboning motor pattern and loading regime, in contrast to shape-function patterns of primates with unfused jaws. All fossil primates examined (except Apidium) exhibit jaw morphologies suggestive of the wishboning motor pattern demonstrated in living anthropoids and indriids. Discussion Partial fusion in Catopithecus, similar to indriids and some subfossil lemurs, may be sufficient to resist, or transfer, some amounts of transversely directed balancing-side muscle force at the symphysis, representing a transition to greater reliance on transverse jaw movement during mastication. Furthermore, possible functional convergences in physiological patterns during chewing (i.e., Archaeolemur) are identified.

Animals that depend on water sources in dry environments must balance their water demands with predation risk. In settings of water scarcity, predators may strategically exploit prey’s dependence on water; prey may adjust their use of water sources either spatially or temporally to avoid overlapping with predators. To examine the spatiotemporal dynamics of predators and prey at water sources, we studied the use of semipermanent waterholes in the dry season by red-fronted lemurs (Eulemur rufifrons), a primate species that exhibits flexible circadian activity patterns and inhabits a dry deciduous forest in western Madagascar. We hypothesized that lemurs avoid predators in their spatiotemporal use of waterholes. We analyzed the patterns of camera trap activations at waterholes by red-fronted lemurs and their two main predators: fossa (Cryptoprocta ferox) and Madagascar harrier hawks (Polyboroides radiatus). We found that red-fronted lemurs were unlikely to use waterholes at times of day when predators were commonly present, and that the distributions of times of waterhole use differed between red-fronted lemurs and each of their predator species. Red-fronted lemurs frequently used waterholes that were also used by predators within the same week in part because the predators used a variable set of water resources. In this system, predators did not appear to exploit waterholes for the high density of red-fronted lemurs attracted to them, but instead likely used waterholes primarily to meet their own water demands. Our findings suggest that when predators and prey share water sources, prey may adjust their behavior to reduce their risk of overlap with predators, including through avoidance of indirect cues of predation, such as waterholes at particular times of day.

Affiliative vocalizations occur across primate taxa and may be used to maintain spatial cohesion and/or to regulate social interactions in group-living species. For gregarious strepsirhines like the ring-tailed lemur (Lemur catta), with large vocal repertoires and several distinct affiliative vocalizations including the chirp and wail, it is important to understand behavioural usage of these vocalizations to gain insight into their social interactions. To determine whether chirp and wail vocalizations facilitate group cohesion, regulate interactions to achieve socially positive outcomes, and are correlated with differences in individual characteristics such as dominance rank and age, I collected 565 h of focal data on 31 males aged ≥1 year at Beza Mahafaly Special Reserve, Madagascar, from March to July 2010. I found that chirp and wail vocalizations occurred at the highest rates during group-wide travel compared to other behaviours. Although nearest neighbour distance did not influence calling rate, focal animals maintained the same distance or were located closer to nearest neighbours after calling. Both chirp and wail calls were heard in behavioural contexts without agonism rather than agonistic contexts. No relationship was found between male calling rate and dominance rank or age, although the chirp showed a non-significant tendency to be produced at higher rates by younger males. Overall, my results indicated that ring-tailed lemur males of all ages and dominance ranks used both chirp and wail vocalizations as contact calls during group-wide travel events, helping individuals maintain proximity to other group members during movement. Chirp and wail vocalizations may additionally help regulate the caller’s social interactions and promote increased tolerance from conspecifics. These findings add to our understanding of the breadth of communication behaviour in wild lemurs, thus furthering our knowledge of the social lives and cognitive abilities of strepsirhines. Through examining the complexity of vocalization use by a living lemur species with a communication system much like early social primates, we gain broad insight into the evolution of primate sociality.

Intergroup encounters are common in nonhuman primates and can vary from affiliative to aggressive. We extracted data from the literature to test five different hypotheses: 1) where there are group size differences between opposing groups, whether the larger group is more likely to win an intergroup encounter than the smaller group; 2) whether the likelihood of a group engaging in aggressive intergroup encounters increases with group size; and 3–5) whether dominant, older individuals, and/or males are more likely to participate aggressively in intergroup encounters than subordinate, younger individuals and/or females. Our data set comprised 52 studies on 31 primate species (3 lemur species, 5 New World monkeys, 19 Old World monkeys, and 4 apes). We found that the larger group is more likely to win an encounter against a smaller group than vice versa. We found no significant relationship between group size and propensity to be aggressive during intergroup encounters. We found weak/no support for the effect of age, dominance rank, and sex on the frequency of aggression displayed toward outgroup individuals during intergroup encounters. Species- and population-specific differences in inter- and intragroup competition and in the degree of the unequal distribution of resources across group members may explain why age, dominance rank, and sex are not strong predictors of aggression during intergroup encounters.

1. Elevation gradients correlate with changes in several environmental conditions and are known to be related to animal abundance. Animals in regions with a naturally limited extent of lowland rainforest are expected to have evolved adaptations to intermediate elevations that provided a stable environment during their evolution. 2. Since the lowland rainforest of Madagascar has a limited extent and suffers from increasing anthropogenic pressure, it is essential to understand how well species tolerate intermediate and high elevations. In this study, we aim to quantify the relationship between lemur abundance and elevation in the eastern rainforest of Madagascar. 3. We correlated abundance data on 26 lemur species (10 genera), including 492 records from 26 studies, with elevation. We analysed the consistency of correlations across species with a meta‐analytical approach. We controlled for species’ body mass, elevational range and median elevation. We then ran generalised linear mixed models to determine whether lemur abundance was related to elevation, body mass, plant productivity and anthropogenic disturbance. 4. Overall, the abundance of lemur species in Malagasy rainforests was negatively correlated with elevation, and species occupying broader elevational ranges showed stronger correlations. Body mass was not related to species’ tolerance of high elevations. Even though several lemur species are able to occupy the entire elevation gradient, the few remaining patches of lowland rainforests host lemur species at greater abundances than other sites. Abundance across species was negatively related to body mass, elevation and seasonality in plant productivity and positively related to plant productivity. 5. Despite the ecological flexibility of many lemur species, the remnant patches of lowland rainforests host the highest levels of lemur abundance and are key to lemur conservation. It is crucial to preserve this priority habitat both for biodiversity conservation and for our understanding of lemur adaptations.

BackgroundGray mouse lemurs (Microcebus murinus) are the smallest and most ancestral primates known. Their size falls in between that of mice and rats, and their genetic proximity to humans makes them an emerging model to study age-related neurodegeneration. Since mouse lemurs replicate similar senescence processes of humans, they constitute a useful model for studying cardiovascular dysfunctions. However, their cardiac physiology is unknown. Thus, we investigated the cardiac pacemaker activity generated by the sinoatrial node (SAN) of mouse lemurs, presenting the first characterization of heart automaticity in nonhuman primates.Methods and ResultsWe recorded cardiac automaticity in mouse lemurs and in their SAN tissues and pacemaker myocytes. Mouse lemurs have a heart rate (HR) in between those of mice and rats and a similar generation of the SAN electrical impulse. Their SAN myocytes express the main pacemaker currents at densities similar to mice: the hyperpolarization-activated current (If) and the L-type (Ica,L) and T-type (Ica,T) calcium currents. Conversely, their ventricular depolarization resembles that of large mammals and despite the small size of mouse lemurs, the total number of heartbeats in their life corresponds to what can be attained by humans.Using muscle-derived stem cells (MDSCs) from mouse lemurs, we also differentiated pacemaker-like (PML) cells showing spontaneous automaticity and expressing markers of native SAN myocytes (HCN4 and connexin-45).ConclusionsOur characterization of heart automaticity in Microcebus murinus provides new opportunities for comparative cardio-physiology studies in primates and with humans and for testing molecules that could modulate age-related dysfunctions of heart rate.

ObjectivesHair (i.e., pelage/fur) is a salient feature of primate (including human) diversity and evolution— serving functions tied to thermoregulation, protection, camouflage, and signaling—but wild primate pelage evolution remains relatively understudied. Specifically, assessing multiple hypotheses across distinct phylogenetic scales is essential but is rarely conducted. We examine whole body hair color and density variation across Indriidae (Avahi, Indri, Propithecus)—a lineage that, like humans, exhibits vertical posture (i.e., their whole bodies are vertical to the sun).Materials and MethodsOur analyses consider multiple phylogenetic scales (family-level, genus-level) and hypotheses (e.g., Gloger’s rule, the body cooling hypotheses). We obtain hair color and density from museum and/or wild animals, opsin genotypes from wild animals, and climate data from WorldClim. To analyze our data, we use phylogenetic generalized linear mixed models (PGLMM) using Markov chain Monte Carlo algorithms.ResultsOur results show that across the Indriidae family, darker hair is typical in wetter regions. However, within Propithecus, dark black hair is common in colder forest regions. Results also show pelage redness increases in populations exhibiting enhanced color vision. Lastly, we find follicle density on the crown and limbs increases in dry and open environments.DiscussionThis study highlights how different selective pressures across distinct phylogenetic scales have likely acted on primate hair evolution. Specifically, our data across Propithecus may implicate thermoregulation and is the first empirical evidence of Bogert’s rule in mammals. Our study also provides rare empirical evidence supporting an early hypothesis on hominin hair evolution.

Vocal communication is an important modality for group-living primates inhabiting dense forest habitats that can hinder visual and olfactory signals. Nevertheless, research on primate vocalizations has historically focused on a narrow subset of haplorhine taxa; comparatively few studies have been focused on strepsirrhines, despite facing similar ecological and social challenges. Ruffed lemurs (Varecia)—a taxon known for their raucous calls—are rainforest specialists that exhibit strong fission–fusion dynamics and communally rear large litters of young. However, surprisingly few studies have examined Varecia vocalizations in the wild, meaning virtually nothing is known about the call types or how they facilitate their unique social and reproductive strategies. Our goal for this study was to examine how various contextual factors such as weather, behavioral state, and subgroup size and composition affected vocal activity across call types in wild black-and-white ruffed lemurs. We conducted focal follows on 31 individuals (two communities) in Mangevo (Ranomafana National Park) from May–August 2019 to record behavioral and vocal activity. We distinguished 11 call types, although three (hum, roar-shriek, chatter) constituted the majority of vocal activity. Calling rates were consistent throughout the day, but decreased with high rainfall. We found sex- and subgroup-specific differences in call usage, likely related to female dominance and subgroup composition, respectively. We identified behavioral contexts that some call types were consistently given in; this can be used to help infer call function. This study provides some of the first quantitative analyses of ruffed lemur vocal communication and lays the groundwork for more systematic hypothesis testing in future studies.

The gray mouse lemur (Microcebus murinus), one of the world's smallest primates, is thought to share a similar ecological niche and many anatomical traits with early euprimates. As a result, it has been considered a suitable model system for early primate physiology and behavior. Moreover, recent studies have demonstrated that mouse lemurs have comparable cognitive abilities and cortical functional organization as haplorhines. Finally, the small brain size of mouse lemurs provides us with actual lower limits for miniaturization of functional brain circuits within the primate clade. Considering its phylogenetic position and early primate-like traits, the mouse lemurs are a perfect model species to study the early evolution of primate brains.

Folivory evolved independently at least three times over the last 40 million years among Madagascar’s lemurs. Many extant lemuriform folivores exist in sympatry in Madagascar’s remaining forests. These species avoid feeding competition by adopting different dietary strategies within folivory, reflected in behavioral, morphological, and microbiota diversity across species. These conditions make lemurs an ideal study system for understanding adaptation to leaf-eating. Most folivorous lemurs are also highly endangered. The significance of folivory for conservation outlook is complex. Though generalist folivores may be relatively well equipped to survive habitat disturbance, specialist folivores occupying narrow dietary niches may be less resilient. Characterizing the genetic bases of adaptation to folivory across species and lineages can provide insights into their differential physiology and potential to resist habitat change. We recently reported accelerated genetic change in RNASE1, a gene encoding an enzyme (RNase 1) involved in molecular adaptation in mammalian folivores, including various monkeys and sifakas (genus Propithecus; family Indriidae). Here, we sought to assess whether other lemurs, including phylogenetically and ecologically diverse folivores, might show parallel adaptive change in RNASE1 that could underlie a capacity for efficient folivory. We characterized RNASE1 in 21 lemur species representing all five families and members of the three extant folivorous lineages: 1) bamboo lemurs (family Lemuridae), 2) sportive lemurs (family Lepilemuridae), and 3) indriids (family Indriidae). We found pervasive sequence change in RNASE1 across all indriids, a dN/dS value > 3 in this clade, and evidence for shared change in isoelectric point, indicating altered enzymatic function. Sportive and bamboo lemurs, in contrast, showed more modest sequence change. The greater change in indriids may reflect a shared strategy emphasizing complex gut morphology and microbiota to facilitate folivory. This case study illustrates how genetic analysis may reveal differences in functional traits that could influence species’ ecology and, in turn, their resilience to habitat change. Moreover, our results support the contention that not all primate folivores are built the same and highlight the need to avoid generalizations about dietary guild in considering conservation outlook, particularly in lemurs where such diversity in folivory has probably led to extensive specialization via niche partitioning.

Summary As chemicals that elicit unlearned, functionally specialized, and species-specific responses [ 1 ] or ‘stereotyped behavior’ [ 2 ], pheromones differ from mammalian scent signatures that comprise complex, variable mixtures, convey multiple messages via learned chemical combinations, and elicit generalized responses [ 1 ]. Studying ring-tailed lemur (Lemur catta) behavior and semiochemistry, a recent study by Shirasu, Ito et al. [ 2 ] claimed to have identified “the first sex pheromones in primates.” However, reliance on one male in most chemical procedures and on few females in behavioral procedures constrains statistical analyses and challenges the broad applicability of their findings. Also, the non-independent testing of even fewer signaler–recipient dyads downplays the critical role of learning and memory in primate communication [ 1 ] — an argument that refuted earlier claims of primate pheromones [ 3 , 4 ]. Here, we challenge each of their four highlighted findings and interpretations.

Environmental enrichment is widely used to improve the quality of life of animals under human care. To successfully implement enrichment programs, it is important to evaluate their effect in different enclosure types since housing conditions may change depending on external factors, such as husbandry, management, or seasonal variation. This study investigates how ring-tailed lemur (Lemur catta) behaviour changes with the availability of enrichment items and the type of enclosure the animals are housed in. Through observations, we compared the behaviour of the lemurs in an indoor and outdoor enclosure, both without and with enrichment items. Although we observed enrichment effects, we found that enclosure type had a bigger effect on the lemurs’ behaviour. Additionally, behavioural changes induced by enrichment items differed between indoor and outdoor enclosures. These results indicate that the effectiveness of enrichment items may depend on the enclosure in which they are provided and consequently suggest that the impact of these programs should not be generalised over enclosure types. This highlights that the evaluation of environmental enrichment programs remains important when optimising zoo animal welfare.

“The Jollies” is a video about the late primate scientist Alison Jolly, narrated by lemurs, a langur monkey, and a dog, whose voices are Jolly’s colleagues, daughter, and Donna Haraway. The...

Background Diversity at the Major Histocompatibility Complex (MHC) is critical to health and fitness, such that MHC genotype may predict an individual’s quality or compatibility as a competitor, ally, or mate. Moreover, because MHC products can influence the components of bodily secretions, an individual’s body odors may signal its MHC composition and influence partner identification or mate choice. Here, we investigated MHC-based signaling and recipient sensitivity by testing for odor-gene covariance and behavioral discrimination of MHC diversity and pairwise dissimilarity in a strepsirrhine primate, the ring-tailed lemur (Lemur catta). Methods First, we coupled genotyping of the MHC class II gene, DRB, with gas chromatography-mass spectrometry of genital gland secretions to investigate if functional genetic diversity is signaled by the chemical diversity of lemur scent secretions. We also assessed if the chemical similarity between individuals correlated with their MHC-DRB similarity. Next, we assessed if lemurs discriminated this chemically encoded, genetic information in opposite-sex conspecifics. Results We found that both sexes signaled overall MHC-DRB diversity and pairwise MHC-DRB similarity via genital secretions, but in a sex- and season-dependent manner. Additionally, the sexes discriminated absolute and relative MHC-DRB diversity in the genital odors of opposite-sex conspecifics, suggesting that lemur genital odors function to advertise genetic quality. Conclusions In summary, genital odors of ring-tailed lemurs provide honest information about an individual’s absolute and relative MHC quality. Complementing evidence in humans and Old World monkeys, we suggest that reliance on scent signals to communicate MHC quality may be important across the primate lineage. Electronic supplementary material The online version of this article (10.1186/s12862-019-1486-0) contains supplementary material, which is available to authorized users.

Auditory, visual and olfactory cues play varying roles in non-human primate communication, and these systems have been intensively studied over the last several decades. The use of vocalisations as a primary mode of communication has been the focus of much research, especially in attempts to understand the origins of human language, with a major focus on anthropoid primates and diurnal lemurs. Over the last decade, technological advances have allowed researchers to begin to conduct in-depth investigations into the communication systems exhibited by the nocturnal and cathemeral prosimian primates, including tarsiers, lemurs and lorises. Understanding how nocturnal prosimians use visual, olfactory and auditory cues is vital for reconstructing the origins of primate communication systems. In this special issue, we highlight some of the more exciting advances in the communication strategies of the prosimians. Contributions come from work conducted in Kenya, Tanzania, Senegal, Rwanda, Madagascar and the Indonesian islands of Java and Sulawesi. Topics will include: the description of novel ultrasonic vocalisations, including frequency and function of these newly discovered calls; the possible use of vocalisations to navigate and assemble at sleep sites; the importance of species-specific contact vocalisations for the identification of new species; the use of urinary and glandular signals to communicate and the methods developed to understand this complex communication in the field; the use of vocalisations for niche separation among nocturnal primates from mainland Africa and Madagascar; and whether or not we can use new technologies to discern whether prosimians use vocalisations for individual identification of group members. We discuss the importance of new field methods including novel equipment and techniques, the use of vocalisation to influence conservation practices and the importance of comparing across prosimian taxa to reconstruct the communication systems of our early primate ancestors.

Primate loud calls often encode information relating to species identity. A previous study of loud calls of fork-marked lemurs (genus Phaner) indicated differences among the calls of four populations that have been accorded species status on the grounds of morphology and biogeography: Phaner electromontis, P. parienti, P. furcifer and P. pallescens. I made field recordings of two typical calls (kiu and kea) emitted by all four populations and conducted playback experiments in Kirindy Forest to investigate whether free-ranging P. pallescens individuals could discriminate the loud calls of their own species from those of others. Individual response behaviour, social context and call type used in playback were analysed using a goodness-of-fit G test. The effect of specific call identity was significant, while the effects of context and call type were not. Individuals responded to P. pallescens calls by approaching the speaker, but not to the calls of other populations. P. pallescens individuals appear to be capable of distinguishing the loud calls of their conspecifics, but the fact that the habitat structure of the sites of recording and playback of P. pallescenscalls was similar sounds a note of caution. Future studies should repeat the experiments with the other populations of fork-marked lemurs.

It has been proposed that primates use advertisement calls exclusively to negotiate spacing, but the function of female calls has rarely been studied. Here, we investigated the function of male and female advertisement calls in the northern giant mouse lemur (Mirza zaza),a non-gregarious nocturnal primate from north-western Madagascar. We recorded advertisement calls and associated behaviours of 35 M. zaza individuals at the Duke University Lemur Center. We found that females of M. zazaexclusively use their advertisement calls to advertise oestrus. In contrast, male advertisement calls appeared to be used in a spacing context. These findings show that primates can use their advertisement calls for both spacing and mate attraction, and that the sexes may differ in how they use these calls. The novel find of females of M. zazaattracting mates with loud advertisement calls contrasts with many non-primate taxa, where acoustic mate attraction is usually a function of male advertisement calls, and with other primates, where females use visual and olfactory cues to attract males. The loud female advertisement calls of M. zaza likely ensure mating success during the short receptive phase in this non-gregariously foraging, nocturnal primate.

Functional studies of skeletal anatomy are predicated on the fundamental assumption that form will follow function. For instance, previous studies have shown that the femora of specialized leaping primates are more robust than those of more generalized primate quadrupeds. Are such differences solely a plastic response to differential loading patterns during postnatal life, or might they also reflect more canalized developmental mechanisms present at birth? Here, we show that perinatal Lemur catta, an arboreal/terrestrial quadruped, have less robust femora than perinatal Propithecus coquereli, a closely related species specialized for vertical clinging and leaping (a highly unusual locomotor mode in which the hindlimbs are used to launch the animal between vertical tree trunks). These results suggest that functional differences in long bone cross-sectional dimensions are manifest at birth, belying simple interpretations of adult postcranial form as a direct record of loading patterns during postnatal life. Despite these significant differences in bone robusticity, we find that hindlimb bone mineralization, material properties, and measures of whole-bone strength generally overlap in perinatal L. catta and P. coquereli, indicating little differentiation in postcranial maturity at birth despite known differences in the pace of craniodental development between the species. In a broader perspective, our results likely reflect evolution acting during prenatal ontogeny. Even though primates are notable for relatively prolonged gestation and postnatal parental care, neonates are not buffered from selection, perhaps especially in the unpredictable and volatile environment of Madagascar. Anat Rec, 2018. © 2018 Wiley Periodicals, Inc. Anat Rec, 303:250-264, 2020. © 2018 American Association for Anatomy.

Sex-biased power structures are common in human and nonhuman primate societies. “Female dominance” is a term applied to a wide range of female-biased power structures. However, the full extent of this variation remains obscure because an adequate vocabulary of power has not been adopted consistently. Female power occurs throughout primates and other animals, even in male-dominant societies, but the legacy of patriarchy persists in primatologists’ use of language and implicit assumptions about intersexual power. While explanations for the occurrence of female power can be accommodated within existing ethological theory, many hypotheses seeking to explain the evolution of female power are narrowly focused on particular taxa. Theories about primate social evolution would benefit from a synthesis of the disparate literature on power, increased emphasis on intersexual social relationships, and comparative studies that include the full behavioral diversity of primates and other mammals.

Habitat degradation and hunting pose the most proximate threats to many primate species, while climate change is expected to exacerbate these threats (habitat and climate change combined henceforth as "global change") and present new challenges. Madagascar's lemurs are earth's most endangered primates, placing added urgency to their conservation in the face of global change. My dissertation focused on the critically endangered golden-crowned sifaka (Propithecus tattersalli; hereafter, "sifaka") which is endemic to fragmented forests across a gradient of dry, moderate, and wet forest types in northeastern Madagascar. I surveyed sifakas across their global range and investigated factors affecting their densities. I explored sifaka diets across different forest types and evaluated if nutritional factors influenced sifaka densities. Lastly, I investigated sifaka range-wide genetic diversity and conducted a connectivity analysis to prioritize corridor-restoration and other potential conservation efforts. Sifaka densities varied widely across forest fragments (6.8 (SE = 2.0-22.8) to 78.1 (SE = 53.1-114.8) sifakas/km²) and populations have declined by as much as 30-43% in 10 years, from ~18,000 to 10,222-12,631 individuals (95% CI: 8,230-15,966). Tree cutting, normalized difference vegetation index (NDVI) during the wet season, and Simpson's diversity index (1-D) predicted sifaka densities range-wide. Sifakas consumed over 101 plant species and spent 27.1% of their active time feeding on buds, flowers, fruits, seeds, and young and mature leaves. Feeding effort and plant part consumption varied by season, forest type, and sex. Minerals in sifaka food items (Mg (β = 0.62, SE = 0.19) and K (β = 0.58, SE = 0.20)) and wet season NDVI (β = 0.43, SE = 0.20) predicted sifaka densities. Genetic measures across forest fragments indicated that sifaka populations are becoming more isolated (moderate FIS values: mean = 0.27, range = 0.11-0.60; high M-ratios: mean = 0.59, range = 0.49-0.82; low overall effective population size: Ne = 139.8-144 sifakas). FST comparisons between fragments (mean = 0.12, range = 0.01-0.30) supported previous findings that sifakas still moved across the fragmented landscape. Further validation of these genetic results is needed. I identified critical corridors that conservation managers could protect and/or expand via active reforestation to ensure the continued existence of this critically-endangered lemur. Doctor of Philosophy Worldwide, many species of primates are threatened with extinction due to habitat degradation, hunting, and climate change (habitat and climate combined threats, henceforth, "global change"). These threats work at different time scales, with hunting being the most immediate and climate change likely to have its fullest impact experienced from the present to a longer time frame. Lemurs are a type of primate found only on Madagascar, an island experiencing rapid global change, which puts lemurs at a heightened risk of extinction. My dissertation research focused on the critically endangered golden-crowned sifaka (Propithecus tattersalli; hereafter, "sifaka"), a species of lemur found only in a few isolated forests across a dry to wet gradient in northeastern Madagascar. To better understand their extinction risk, I conducted surveys to estimate the number of sifakas remaining and investigated several factors that might determine how many sifakas can live in one place. I then explored how sifaka diets varied depending on the forest type that they inhabit and tested whether nutrients in their food might determine sifaka numbers. Lastly, I calculated sifaka genetic diversity to assess their ability to adapt to new environmental conditions and to determine whether sifakas can move across the landscape to find new mates and to potentially colonize new areas of habitat. Sifaka densities varied widely across their range (6.8-78.1 sifakas/km² ). Only 10,222-12,631 sifakas remain, which is 30-43% less than the range of estimates obtained 10 years ago (~18,000 sifakas). Tree cutting, normalized difference vegetation index (NDVI; a measure of plant health or "greenness" obtained from satellite data), and a tree species diversity index were useful measures to predict sifaka densities. Sifakas ate different plant parts (buds, flowers, fruits, seeds, and leaves) from over 101 plant species. The amount of time they spent eating each day varied by the time of year, forest type, and sex. On average, they spent a quarter of their day eating. Magnesium and potassium concentrations in sifaka food items also were useful nutrition-related measures to predict sifaka densities. Genetic analyses suggested that sifaka populations are becoming more isolated and inbred, meaning sifakas are breeding with other sifakas to which they are closely related. However, it appears that sifakas still can move between forest patches to find new mates and to potentially colonize new areas, if such areas are created. Further validation of these genetic results is needed. I also identified critical areas that will be important to protect and reforest to ensure that movements between populations can continue.

Contemporary theory that emphasizes the roles of oxytocin and vasopressin in mammalian sociality has been shaped by seminal vole research that revealed interspecific variation in neuroendocrine circuitry by mating system. However, substantial challenges exist in interpreting and translating these rodent findings to other mammalian groups, including humans, making research on nonhuman primates crucial. Both monogamous and non-monogamous species exist within Eulemur, a genus of strepsirrhine primate, offering a rare opportunity to broaden a comparative perspective on oxytocin and vasopressin neurocircuitry with increased evolutionary relevance to humans. We performed oxytocin and arginine vasopressin 1a receptor autoradiography on 12 Eulemur brains from seven closely related species to (1) characterize receptor distributions across the genus, and (2) examine differences between monogamous and non-monogamous species in regions part of putative “pair-bonding circuits”. We find some binding patterns across Eulemur reminiscent of olfactory-guided rodents, but others congruent with more visually oriented anthropoids, consistent with lemurs occupying an ‘intermediary’ evolutionary niche between haplorhine primates and other mammalian groups. We find little evidence of a “pair-bonding circuit” in Eulemur akin to those proposed in previous rodent or primate research. Mapping neuropeptide receptors in these nontraditional species questions existing assumptions and informs proposed evolutionary explanations about the biological bases of monogamy.

International audience; Orientation preference maps (OPMs) are a prominent feature of primary visual cortex (V1) organization in many primates and carnivores. In rodents, neurons are not organized in OPMs but are instead interspersed in a ‘‘salt and pepper’’ fashion, although clusters of orientation-selective neurons have been reported. Does this fundamental difference reflect the existence of a lower size limit for orientation columns (OCs) below which they cannot be scaled down with decreasing V1 size? To address this question, we examined V1 of one of the smallest living primates, the 60-g prosimian mouse lemur (Microcebus murinus). Using chronic intrinsic signal imaging, we found that mouse lemur V1 contains robust OCs, which are arranged in a pinwheel-like fashion. OC size in mouse lemurs was found to be only marginally smaller compared to the macaque, suggesting that these circuit elements are nearly incompressible. The spatial arrangement of pinwheels is well described by a common mathematical design of primate V1 circuit organization. In order to accommodate OPMs, we found that the mouse lemur V1 covers one-fifth of the cortical surface, which is one of the largest V1-to-cortex ratios found in primates. These results indicate that the primate-type visual cortical circuit organization is constrained by a size limitation and raises the possibility that its emergence might have evolved by disruptive innovation rather than gradual change.

Versión preprint disponible en: http://hdl.handle.net/10261/229066, The novel coronavirus SARS‐CoV‐2, which in humans leads to the disease COVID‐19, has caused global disruption and more than 2 million fatalities since it first emerged in late 2019. As we write, infection rates are at their highest point globally and are rising extremely rapidly in some areas due to more infectious variants. The primary target of SARS‐CoV‐2 is the cellular receptor angiotensin‐converting enzyme‐2 (ACE2). Recent sequence analyses of the ACE2 gene predict that many nonhuman primates are also likely to be highly susceptible to infection. However, the anticipated risk is not equal across the Order. Furthermore, some taxonomic groups show high ACE2 amino acid conservation, while others exhibit high variability at this locus. As an example of the latter, analyses of strepsirrhine primate ACE2 sequences to date indicate large variation among lemurs and lorises compared to other primate clades despite low sampling effort. Here, we report ACE2 gene and protein sequences for 71 individual strepsirrhines, spanning 51 species and 19 genera. Our study reinforces previous results while finding additional variability in other strepsirrhine species, and suggests several clades of lemurs have high potential susceptibility to SARS‐CoV‐2 infection. Troublingly, some species, including the rare and endangered aye‐aye (Daubentonia madagascariensis), as well as those in the genera Avahi and Propithecus, may be at high risk. Given that lemurs are endemic to Madagascar and among the primates at highest risk of extinction globally, further understanding of the potential threat of COVID‐19 to their health should be a conservation priority. All feasible actions should be taken to limit their exposure to SARS‐CoV‐2., ADM is supported bythe Natural Sciences and Engineering Research Council of Canada(NSERC Discovery Grant) and Canada Research Chairs Program.MCJ's postdoctoral appointment is supported by funding from theNatural Environment Research Council (NERC NE/T000341/1). IGand MG acknowledge the support of the Spanish Ministry of Scienceand Innovation through the Instituto de Salud Carlos III and the2014–2020 Smart Growth Operating Program, to the EMBL part-nership and cofinancing with the European Regional DevelopmentFund (MINECO/FEDER, BIO201571792P). We also acknowledgethe support of the Centro de Excelencia Severo Ochoa, and theGeneralitat de Catalunya through the Departament de Salut, De-partament d'Empresa i Coneixement and the CERCA Programme.TMB is supported by funding from the European Research Council(ERC) under the European Union's Horizon 2020 research and in-novation program (grant agreement No. 864203), BFU201786471P (MINECO/FEDER, UE), “Unidad de Excelencia María de Maeztu”,funded by the AEI (CEX2018000792M), Howard Hughes Interna-tional Early Career, Obra Social "La Caixa" and Secretaria d'Uni-versitats i Recerca and CERCA Programme del Departamentd'Economia i Coneixement de la Generalitat de Catalunya (GRC2017 SGR 880). PSA thanks the National Institutes of Health(R35GM130333) for financial support. EL is supported by CGL201782654P (MINECO/FEDER, UE). EDJ and OF's contributions weresupported by funds from Howard Hughes Medical Institute and theRockefeller University. Chris Smith drew the images for Figure 1. Theauthors would like to thank the Veterinary and Zoology staff atWildlife Reserves Singapore for their help in obtaining the tissuesamples, as well as the Lee Kong Chian Natural History Museum forstorage and provision of the tissue samples. Finally, we thank tworeviewers for quick and constructive comments, and Karen Bales forher supportive editorial oversight

Evidence suggests venomous snakes and primates have evolved certain traits in response to a coevolutionary arms-race. In both clades, evolved traits include an increase in brain size and enhanced vision. Lineage specific traits include in primates an inherent fear of snakes, while cobras have evolved defensive toxins, hooding, aposematism and venom spitting. To strengthen the claims of coevolution between venomous snakes and primates, more evidence of coevolved traits is needed to highlight the importance of this arms-race. We report a significantly reduced susceptibility of snake venom α-neurotoxins toward the α-1 nicotinic acetylcholine receptor orthosteric site within the catarrhine primates. This trait is particularly amplified within the clade Homininae. This relationship is supported by post-synaptic neurotoxic symptoms of envenoming relative to prey species being much lower humans due to weak binding of α-neurotoxins to human nicotinic receptors. Catarrhines are sympatric with many species of large, diurnal, neurotoxically venomous snakes and as such are likely to have had a long history of interaction with them. Conversely, the Lemuriformes and Platyrrhini are highly susceptible to binding of α-neurotoxins, which is consistent with them occupying geographical locations either devoid of venomous snakes or areas with neurotoxic snakes that are small, fossorial, and nocturnal. These data are consistent with the snake detection theory in that they follow a similar pattern of evolved traits within specific primate clades that are sympatric with venomous snakes. These results add new strong evidence in support of snakes and primates coevolving through arms-races that shaped selection pressures for both lineages.Significance StatementWe have discovered a pattern of primate susceptibility towards α-neurotoxins that supports the theory of a coevolutionary arms-race between venomous snakes and primates.

Arthropods (insects, spiders, etc.) can fulfill major nutritional requirements for primates, particularly in terms of proteins, fats, vitamins, and minerals. Yet, for many primate species we know very little about the frequency and importance of arthropod consumption. Traditional methods for arthropod prey identification, such as behavioral observations and fecal dissections, offer limited taxonomic resolution and, as a result, underestimate true diversity. Metabarcoding arthropod DNA from primate fecal samples provides a promising but underused alternative. Here, we inventoried arthropod prey diversity in wild lemurs by sequencing two regions of the CO1 gene. Samples were collected opportunistically from 10 species of lemurs inhabiting three national parks in southern Madagascar using a combination of focal animal follows and live trapping. In total, we detected arthropod DNA in 98 of the 170 fecal samples analyzed. Although all lemur species included in these analyses showed evidence of arthropod consumption, those within the family Cheirogaleidae appeared to consume the highest frequency and diversity of arthropods. To our knowledge, this study presents the first evidence of arthropod consumption in Phaner pallescens, Avahi peyrierasi, and Propithecus verreauxi, and identifies 32 families of arthropods as probable food items that have not been published as lemur dietary items to date. Our study emphasizes the importance of arthropods as a nutritional source and the role DNA metabarcoding can play in elucidating an animal's diet.

International audience; In arboreal environments, substrate orientation determines the biomechanical strategy for postural maintenance and locomotion. In this study, we investigated possible neuronal correlates of these mechanisms in an ancestral primate model, the gray mouse lemur. We conducted telemetric recordings of electrocorticographic activity in left primary motor cortex of two mouse lemurs moving on a branch-like small-diameter pole, fixed horizontally, or vertically. Analysis of cortical oscillations in high β (25-35 Hz) and low γ (35-50 Hz) bands showed stronger resting power on horizontal than vertical substrate, potentially illustrating sensorimotor processes for postural maintenance. Locomotion on horizontal substrate was associated with stronger event-related desynchronization than vertical substrate, which could relate to locomotor adjustments and/or derive from differences in baseline activity. Spectrograms of cortical activity showed modulation throughout individual locomotor cycles, with higher values in the first than second half cycle. However, substrate orientation did not significantly influence these variations. Overall, these results confirm that specific cortical mechanisms are solicited during arboreal locomotion, whereby mouse lemurs adjust cortical activity to substrate orientation during static posture and locomotion, and modulate this activity throughout locomotor cycles.