Orientation Preference Maps in Microcebus murinus Reveal Size-Invariant Design Principles in Primate Visual Cortex.

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.

Ecology and morphology of mouse lemurs (Microcebus spp.) in a hotspot of microendemism in northeastern Madagascar, with the description of a new species.

Delimitation of cryptic species is increasingly based on genetic analyses but the integration of distributional, morphological, behavioral, and ecological data offers unique complementary insights into species diversification. We surveyed communities of nocturnal mouse lemurs (Microcebus spp.) in five different sites of northeastern Madagascar, measuring a variety of morphological parameters and assessing reproductive states for 123 individuals belonging to five different lineages. We documented two different non-sister lineages occurring in sympatry in two areas. In both cases, sympatric species pairs consisted of a locally restricted (M. macarthurii or M. sp. #3) and a more widespread lineage (M. mittermeieri or M. lehilahytsara). Estimated Extents of Occurrence (EOO) of these lineages differed remarkably with 560 and 1,500 km2 versus 9,250 and 50,700 km2 , respectively. Morphometric analyses distinguished unambiguously between sympatric species and detected more subtle but significant differences among sister lineages. Tail length and body size were most informative in this regard. Reproductive schedules were highly variable among lineages, most likely impacted by phylogenetic relatedness and environmental variables. While sympatric species pairs differed in their reproductive timing (M. sp. #3/M. lehilahytsara and M. macarthurii/M. mittermeieri), warmer lowland rainforests were associated with a less seasonal reproductive schedule for M. mittermeieri and M. lehilahytsara compared with populations occurring in montane forests. Distributional, morphological, and ecological data gathered in this study support the results of genomic species delimitation analyses conducted in a companion study, which identified one lineage, M. sp. #3, as meriting formal description as a new species. Consequently, a formal species description is included. Worryingly, our data also show that geographically restricted populations of M. sp. #3 and its sister species (M. macarthurii) are at high risk of local and perhaps permanent extinction from both deforestation and habitat fragmentation.

The evolution of palate shape in the Lepilemur-Cheirogaleidae clade (Primates: Strepsirrhini).

OBJECTIVES: Phylogenies consistently group the folivorous Lepilemur species with the small-bodied insectivorous-frugivorous cheirogaleids. Juvenile lepilemurs and adult cheirogaleids share allometries in most aspects of skull morphology, except the palate. We investigated potential influences on palate shape in these taxa and several outgroups using geometric morphometrics. MATERIALS AND METHODS: Our sample included representatives of four extant strepsirrhine families, Cheirogaleidae (including Lepilemurinae), Lemuridae, Indriidae, and Galagidae, and one subfossil Megaladapis. Our dataset comprised 32 landmarks collected from 397 specimens representing 15 genera and 28 species, and was analyzed using generalized procrustes analyses and between group principal component analysis. We explored the influence of size, phylogeny, diet, and the propagation of loud vocalizations on palate shape. RESULTS: While congeneric species clustered within the morphospace, the phylomorphospace did not mirror molecular phylogenetic hypotheses of higher-order relationships. Four palate forms were distinguished within the Cheirogaleidae. Diet, strongly linked to body size, had the single greatest influence on palate shape. The production of long-distance advertisement calls was most often associated with positive scores on the PC1 axis. DISCUSSION: Our results suggest that the extensive variation in palate shape among Cheirogaleidae is related to dietary shifts that accompanied changes in body size during the clade's radiation. Molecular phylogenies indicate that cheirogaleid diversification involved repeated dwarfing events, which in turn drove dietary shifts from ancestral folivory-frugivory to frugivory, gummivory, and faunivory in the descendant species. The elongated Lepilemur palate is probably related to accelerated eruption of the cheek teeth to render juveniles competent to shear leaves upon weaning.

The Forearm Musculature of the Gray Mouse Lemur (Microcebus murinus): An Ontogenetic Study.

Although studies have sought to characterize variation in forearm muscular anatomy across the primate order, none have attempted to quantify ontogenetic changes in forearm myology within a single taxon. Herein, we present muscle architecture data for the forearm musculature (flexors and extensors of the wrist and digits) of Microcebus murinus, a small Lemuroid that has been the focus of several developmental studies. A quadratic curvilinear model described ontogenetic changes in muscle mass and fascicle length; however, fascicle lengths reached peak levels at an earlier age and showed a stronger decline during senescence. Conversely, physiological cross-sectional area followed a more linear trend, increasing steadily throughout life. As previous studies into the functional role of the primate forelimb emphasize the importance of long muscle fascicles within arboreal taxa in order to maximize mobility and flexibility, the early attainment of peak fascicle lengths may consequently reflect the importance of agility within this mobile and highly arboreal species. Similarly, observed myological trends in forearm strength are supported by previous in vivo data on grip strength within M. murinus in which senescent individuals showed no decline in forearm force relative to prime age individuals. This trend is interpreted to reflect compensation for the previously reported decline in hind limb grip strength in the hind limb with age, such that older individuals are able to maintain arboreal stability. Interestingly, the ontogenetic trajectory of each architectural variable mirrored previous observations of the masticatory musculature in M. murinus, suggesting that ontogenetic trends are relatively conserved between anatomical regions. Anat Rec, 303:1354-1363, 2020. © 2019 American Association for Anatomy.

The Ontogeny of Masticatory Muscle Architecture in Microcebus murinus.

The masticatory apparatus has been the focus of many studies in comparative anatomy-especially analyses of skulls and teeth, but also of the mandibular adductor muscles which are responsible for the production of bite force and the movements of the mandible during food processing and transport. The fiber architecture of these muscles has been correlated to specific diets (e.g., prey size in felids) and modes of foraging (e.g., tree gouging in marmosets). Despite the well-elucidated functional implications of this architecture, little is known about its ontogeny. To characterize age-related myological changes, we studied the masticatory muscles in a large (n = 33) intraspecific sample of a small, Malagasy primate, Microcebus murinus including neonatal through geriatric individuals. We removed each of the mandibular adductors and recorded its mass as well as other linear measurements. We then chemically dissected each muscle to study its architecture-fascicle length and physiological cross-sectional area (PCSA) which relate to stretch (gape) and force capabilities, respectively. We observed PCSA and muscle mass to increase rapidly and plateau in adulthood through senescence. Fascicle lengths remained relatively constant once maximal length was reached, which occurred early in life, suggesting that subsequent changes in PCSA are driven by changes in muscle mass. Quadratic curvilinear models of each of the architectural variables of all adductors combined as well as individual muscles regressed against age were all significant. Anat Rec, 303:1364-1373, 2020. © 2019 American Association for Anatomy.

Genetic and morphological diversity of mouse lemurs (Microcebus spp.) in northern Madagascar: The discovery of a putative new species?

Tropical forests harbor extremely high levels of biological diversity and are quickly disappearing. Despite the increasingly recognized high rate of habitat loss, it is expected that new species will be discovered as more effort is put to document tropical biodiversity. Exploring under-studied regions is particularly urgent if we consider the rapid changes in habitat due to anthropogenic activities. Madagascar is known for its extraordinary biological diversity and endemicity. It is also threatened by habitat loss and fragmentation. It holds more than 100 endemic primate species (lemurs). Among these, Microcebus (mouse lemurs) is one of the more diverse genera. We sampled mouse lemurs from several sites across northern Madagascar, including forests never sampled before. We obtained morphological data from 99 Microcebus individuals; we extracted DNA from tissue samples of 42 individuals and amplified two mitochondrial loci (cytb and cox2) commonly used for species identification. Our findings update the distribution of three species (Microcebus tavaratra, Microcebus arnholdi, and Microcebus mamiratra), including a major increase in the distribution area of M. arnholdi. We also report the discovery of a new Microcebus lineage genetically related to M. arnholdi. Several complementary approaches suggest that the newly identified Microcebus lineage might correspond to a new putative species, to be confirmed or rejected with additional data. In addition, morphological analyses showed (a) clear phenotypic differences between M. tavaratra and M. arnholdi, but no clear differences between the new Microcebus lineage and the sister species M. arnholdi; and (b) a significant correlation between climatic variables and morphology, suggesting a possible relationship between species identity, morphology, and environment. By integrating morphological, climatic, genetic, and spatial data of two northern Microcebus species, we show that the spatial distribution of forest-dwelling species may be used as a proxy to reconstruct the past spatial changes in forest cover and vegetation type.

The sensory thalamus and visual midbrain in mouse lemurs.

Mouse lemurs are the smallest of extant primates and are thought to resemble early primates in many ways. We provide histological descriptions of the major sensory nuclei of the dorsal thalamus and the superior colliculus (SC) of mouse lemurs (Microcebus murinus). The dorsal lateral geniculate nucleus has the six layers typical of strepsirrhine primates, with matching pairs of magnocellular, parvocellular, and koniocellular layers, one of each pair for each eye. Unlike most primates, magnocellular and parvocellular layers exhibit only small differences in cell size. All layers express vesicular glutamate transporter 2 (VGLUT2), reflecting terminations of retinal inputs, and the expression of VGLUT2 is much less dense in the koniocellular layers. Parvalbumin is densely expressed in all layers, while SMI-32 is densely expressed only in the magnocellular layers. The adjoining pulvinar complex has a posterior nucleus with strong VGLUT2 expression, reflecting terminations from the SC. The SC is laminated with dense expression of VGLUT2 in the upper superficial gray layer, reflecting terminations from the retina. The ventral (MGNv), medial, and dorsal divisions of the medial geniculate complex are only moderately differentiated, although patches of dense VGLUT2 expression are found along the outer border of MGNv. The ventroposterior nucleus has darkly stained cells in Nissl stained sections, and narrow septa separating patchy regions of dense VGLUT2 expression that likely represent different body parts. Overall, these structures resemble those in other strepsirrhine primates, although they are smaller, with the sensory nuclei appearing to occupy proportionately more of the dorsal thalamus than in larger primates.

A 3D population-based brain atlas of the mouse lemur primate with examples of applications in aging studies and comparative anatomy.

The gray mouse lemur (Microcebus murinus) is a small prosimian of growing interest for studies of primate biology and evolution, and notably as a model organism of brain aging. As brain atlases are essential tools for brain investigation, the objective of the current work was to create the first 3D digital atlas of the mouse lemur brain. For this, a template image was constructed from in vivo magnetic resonance imaging (MRI) data of 34 animals. This template was then manually segmented into 40 cortical, 74 subcortical and 6 cerebro-spinal fluid (CSF) regions. Additionally, we generated probability maps of gray matter, white matter and CSF. The template, manual segmentation and probability maps, as well as imaging tools used to create and manipulate the template, can all be freely downloaded. The atlas was first used to automatically assess regional age-associated cerebral atrophy in a cohort of mouse lemurs previously studied by voxel based morphometry (VBM). Results based on the atlas were in good agreement with the VBM ones, showing age-associated atrophy in the same brain regions such as the insular, parietal or occipital cortices as well as the thalamus or hypothalamus. The atlas was also used as a tool for comparative neuroanatomy. To begin with, we compared measurements of brain regions in our MRI data with histology-based measures from a reference article largely used in previous comparative neuroanatomy studies. We found large discrepancies between our MRI-based data and those of the reference histology-based article. Next, regional brain volumes were compared amongst the mouse lemur and several other mammalian species where high quality volumetric MRI brain atlases were available, including rodents (mouse, rat) and primates (marmoset, macaque, and human). Unlike those based on histological atlases, measures from MRI atlases indicated similar cortical to cerebral volume indices in all primates, including in mouse lemurs, and lower values in mice. On the other hand, white matter to cerebral volume index increased from rodents to small primates (mouse lemurs and marmosets) to macaque, reaching their highest values in humans.

Spontaneous Spongiform Brainstem Degeneration in a Young Mouse Lemur (Microcebus murinus) with Conspicuous Behavioral, Motor, Growth, and Ocular Pathologies.

Here we report a case of severe growth retardation and neurologic abnormalities in a female gray mouse lemur (Microcebus murinus), a small NHP species for which the genomic sequence recently became available. The female lemur we present here died on postnatal day 125. This lemur had impaired development of motor skills and showed severe ataxia and tremors. In addition, hearing seemed normal whereas ophthalmic examination revealed incipient bilateral cataracts, abnormal pigmentation in the lens of the left eye, and a missing optokinetic nystagmus, which indicated impaired vision. Most prominently, the lemur showed severe growth retardation. Necropsy revealed maldevelopment of the left reproductive organs and unilateral dilation of the right lateral ventricle, which was confirmed on brain MRI. Brain histology further revealed large, bilateral areas of vacuolation within the brainstem, but immunohistochemistry indicated no sign of pathologic prion protein deposition. Full genomic sequencing of the lemur revealed a probably pathologic mutation in LARGE2 of the LARGE gene family, which has been associated with congenital muscular dystrophies. However, potentially functional mutations in other genes were also present. The observed behavioral and motor signs in the presented animal might have been linked to spongiform degeneration and resulting brainstem dysfunction and progressive muscle weakness. The macroscopic developmental abnormalities and ophthalmic findings might be genetic in origin and linked to the mutation in LARGE2.

Discovery of an island population of dwarf lemurs (Cheirogaleidae: Cheirogaleus) on Nosy Hara, far northern Madagascar.

The species-level diversity of Madagascar's lemurs has increased hugely over the last two decades, growing from 32 species in 1994 to 102 species in 2014. This growth is primarily due to the application of molecular phylogenetic analyses and the phylogenetic species concept to known populations, and few previously unknown lemur populations have been discovered during this time. We report on a new population of dwarf lemurs (Cheirogaleus sp.) from Nosy Hara, a 312-ha island in far northern Madagascar, which constitutes the northernmost distribution record for the genus. The dwarf lemurs appeared to show two characteristics of island populations-insular dwarfism and predator naïveté-that suggest a long isolation, and may thus represent an undescribed taxon. If this is the case, the dwarf lemurs of Nosy Hara are probably one of the rarest primate taxa on Earth.

Nasal morphometry in marmosets: loss and redistribution of olfactory surface area.

The two major groups of primates differ in internal nasal anatomy. Strepsirrhines (e.g., lemurs) have more numerous turbinals and recesses compared with haplorhines (e.g., monkeys). Since detailed quantitative comparisons of nasal surface area (SA) have not been made, we measured mucosa in serially sectioned monkeys (Callithrix jacchus, Cebuella pygmaea). Data were compared with previously published findings on the mouse lemur, Microcebus murinus. The nasal airways were digitally reconstructed using computed tomography scanned heads of Cebuella and Microcebus. In addition, morphometric and functional analyses were carried out using segmented photographs of the histological sections of Cebuella and Microcebus. The SA of the ethmoturbinal complex is about half as large in marmosets compared with Microcebus, and is covered with less olfactory mucosa (18%-24% in marmosets, compared with ∼ 50% in Microcebus). Whereas the ethmoturbinal complex of Microcebus bears half of the total olfactory mucosa in the nasal airway, most (∼ 80%) olfactory mucosa is distributed on other surfaces in the marmosets (e.g., nasal septum). A comparison to previously published data suggests all primate species have less olfactory surface area (OSA) compared with other similar-sized mammals, but this is especially true of marmosets. Taken together, these findings support the hypothesis that there is a reduced OSA in at least some haplorhines, and this can be linked to diminished posterosuperior dimensions of the nasal fossae. However, haplorhines may have minimized their olfactory loss by redistributing olfactory mucosa on non-turbinal surfaces. Our findings also imply that airflow patterns in the olfactory region differ among primates.

Species concepts, diversity, and evolution in primates: lessons to be learned from mouse lemurs.

Humans primarily rely on vision when categorizing the world. If you just look at the same-sized but strikingly differently colored Neotropical poison-dart frogs such as strawberry frogs (Fig. ), you would be convinced that they must belong to different species. However, this is an excellent example of a polymorphic species, meaning that although these frogs look quite different, mating decisions are made based on their conspicuous and species-specific advertisements calls, which are not primarily linked to specific color pattern. The situation is quite different among nocturnal primates living in dense forest environments, such as the tiny nocturnal Malagasy mouse lemurs. In this case, even geographically isolated, well-accepted species look superficially quite similar and are therefore often termed cryptic species (Fig. ). Some morphs are a bit larger than others or show minor phenotypic differences, but morph-specific differences are difficult to detect in living subjects. This phenomenon explains why, until the end of the last century, species diversity in mouse lemurs was assumed to be low, with only two morphologically distinct species. Over the last two decades, several international working groups, including our own, undertook a massive island-wide sampling effort, including DNA sequencing and phylogenetic analyses of mouse lemurs. These revealed a 10-fold higher species diversity, with 21 currently described species. Are these new species, mostly defined based on the phylogenetic species concept (sensu Cracraft), or independent evolutionary lineages or, perhaps, only artifacts of taxonomic inflation? What is a species? How can we identify primate species? How and why do species emerge during evolution?

Functional and evolutionary aspects of axial stability in euarchontans and other mammals.

The presence of a stable thoracolumbar region, found in many arboreal mammals, is considered advantageous for bridging and cantilevering between discontinuous branches. However, no study has directly explored the link between osteological features cited as enhancing axial stability and the frequency of cantilevering and bridging behaviors in a terminal branch environment. To fill this gap, we collected metric data on costal and vertebral morphology of primate and nonprimate mammals known to cantilever and bridge frequently and those that do not. We also quantified the frequency and duration of cantilevering and bridging behaviors using experimental setups for species that have been reported to show differences in use of small branches and back anatomy (Caluromys philander, Loris tardigradus, Monodelphis domestica, and Cheirogaleus medius). Phylogenetically corrected principal component analysis reveals that taxa employing frequent bridging and cantilevering (C. philander and lorises) also exhibit reduced intervertebral and intercostal spaces, which can serve to increase thoracolumbar stability, when compared to closely related species (M. domestica and C. medius). We observed C. philander cantilevering and bridging significantly more often than M. domestica, which never cantilevered or crossed any arboreal gaps. Although no difference in the frequency of cantilevering was observed between L. tardigradus and C. medius, the duration of cantilevering bouts was significantly greater in L. tardigradus. These data suggest that osteological features promoting axial rigidity may be part of a morpho-behavioral complex that increases stability in mammals moving and foraging in a terminal branch environment.

Edge effects on morphometrics and body mass in two sympatric species of mouse lemurs in Madagascar.

Edge effects are an inevitable and important consequence of forest loss and fragmentation. These effects include changes in species biology and biogeography. Here we examine variations in body mass and morphometrics for 2 sympatric species of mouse lemurs (Microcebus murinus and M. ravelobensis) between edge and interior habitats in the dry deciduous forest at Ankarafantsika National Park. Between May and August 2012, we conducted mark-recapture experiments on mouse lemurs trapped along edge and interior forest transects within continuous forest adjacent to a large savannah. Of the 34 M. murinus captured during our study, 82% (n = 28) were trapped in interior habitats. Conversely, 72% (n = 47) of M. ravelobensis were captured in edge habitats. We found that mean body mass of M. murinus and M. ravelobensis did not differ between edge and interior habitats. However, female M. ravelobensis weighed significantly more in edge habitats (56.09 ± 1.74 g) than in interior habitats (48.14 ± 4.44 g). Our study provides some of the first evidence of sex differences in edge responses for a primate species.

The oldest known primate skeleton and early haplorhine evolution.

Reconstructing the earliest phases of primate evolution has been impeded by gaps in the fossil record, so that disagreements persist regarding the palaeobiology and phylogenetic relationships of the earliest primates. Here we report the discovery of a nearly complete and partly articulated skeleton of a primitive haplorhine primate from the early Eocene of China, about 55 million years ago, the oldest fossil primate of this quality ever recovered. Coupled with detailed morphological examination using propagation phase contrast X-ray synchrotron microtomography, our phylogenetic analysis based on total available evidence indicates that this fossil is the most basal known member of the tarsiiform clade. In addition to providing further support for an early dichotomy between the strepsirrhine and haplorhine clades, this new primate further constrains the age of divergence between tarsiiforms and anthropoids. It also strengthens the hypothesis that the earliest primates were probably diurnal, arboreal and primarily insectivorous mammals the size of modern pygmy mouse lemurs.

Biological variation in a large sample of mouse lemurs from Amboasary, Madagascar: implications for interpreting variation in primate biology and paleobiology.

A thorough knowledge of biological variation in extant primates is imperative for interpreting variation, and for delineating species in primate biology and paleobiology. This is especially the case given the recent, rapid taxonomic expansion in many primate groups, notably among small-bodied nocturnal forms. Here we present data on dental, cranial, and pelage variation in a single-locality museum sample of mouse lemurs from Amboasary, Madagascar. To interpret these data, we include comparative information from other museum samples, and from a newly collected mouse lemur skeletal sample from the Beza Mahafaly Special Reserve (BMSR), Madagascar. We scored forty dental traits (n = 126) and three pelage variants (n = 19), and collected 21 cranial/dental measures. Most dental traits exhibit variable frequencies, with some only rarely present. Individual dental variants include misshapen and supernumerary teeth. All Amboasary pelage specimens display a "reversed V" on the cap, and a distinct dorsal median stripe on the back. All but two displayed the dominant gray-brown pelage coloration typical of Microcebus griseorufus. Cranial and dental metric variability are each quite low, and craniometric variation does not illustrate heteroscedasticity. To assess whether this sample represents a single species, we compared dental and pelage variation to a documented, single-species M. griseorufus sample from BMSR. As at Amboasary, BMSR mouse lemurs display limited odontometric variation and wide variation in non-metric dental traits. In contrast, BMSR mouse lemurs display diverse pelage, despite reported genetic homogeneity. Ranges of dental and pelage variation at BMSR and Amboasary overlap. Thus, we conclude that the Amboasary mouse lemurs represent a single species - most likely (in the absence of genetic data to the contrary) M. griseorufus, and we reject their previous allocation to Microcebus murinus. Patterns of variation in the Amboasary sample provide a comparative template for recognizing the degree of variation manifested in a single primate population, and by implication, they provide minimum values for this species' intraspecific variation. Finally, discordance between different biological systems in our mouse lemur samples illustrates the need to examine multiple systems when conducting taxonomic analyses among living or fossil primates.

Lemur habitat and dental senescence in Ranomafana National Park, Madagascar.

Not only can teeth provide clues about diet, but they also can be indicators of habitat quality. Conspecific groups living in different habitats with different kinds of foods may exhibit different rates of dental attrition because their teeth are less well adapted to some foods than to others. Ecological disequilibrium describes the situation in which animals live in habitats to which they are relatively poorly adapted. We test whether dental senescence, the wear-related decrease in dental functionality that is associated with decreased survival of infants born to older Propithecus edwardsi females, can be explained by ecological disequilibrium. Specifically, we compare the rates of dental wear in sifaka groups living in nearby habitats that differ in the degree of anthropogenically induced disturbance. We hypothesize that sifakas living in disturbed areas have an unusual rate of tooth wear compared to those living in a more pristine area, and that dental senescence is a consequence of an atypically high wear rate in a degraded habitat. To test whether habitat quality affects tooth wear more generally, we compare rates of use-wear in two subsets of Microcebus rufus living in either relatively undisturbed or disturbed habitats. Contrary to our predictions, we did not detect different rates of tooth wear in disturbed versus undisturbed habitats for either species and consider that reproductively detrimental dental senescence in P. edwardsi females is unlikely to be a pathological consequence of ecological disequilibrium.

Convenience polyandry or convenience polygyny? Costly sex under female control in a promiscuous primate.

Classic sex roles depict females as choosy, but polyandry is widespread. Empirical attempts to understand the evolution of polyandry have often focused on its adaptive value to females, whereas 'convenience polyandry' might simply decrease the costs of sexual harassment. We tested whether constraint-free female strategies favour promiscuity over mating selectivity through an original experimental design. We investigated variation in mating behaviour in response to a reversible alteration of sexual dimorphism in body mass in the grey mouse lemur, a small primate where female brief sexual receptivity allows quantifying polyandry. We manipulated body condition in captive females, predicting that convenience polyandry would increase when females are weaker than males, thus less likely to resist their solicitations. Our results rather support the alternative hypothesis of 'adaptive polyandry': females in better condition are more polyandrous. Furthermore, we reveal that multiple mating incurs significant energetic costs, which are strikingly symmetrical between the sexes. Our study shows that mouse lemur females exert tight control over mating and actively seek multiple mates. The benefits of remating are nevertheless not offset by its costs in low-condition females, suggesting that polyandry is a flexible strategy yielding moderate fitness benefits in this small mammal.

Distribution of olfactory and nonolfactory surface area in the nasal fossa of Microcebus murinus: implications for microcomputed tomography and airflow studies.

The nasal fossa of most mammals exemplifies extreme skeletal complexity. Thin scrolls of bone (turbinals) that both elaborate surface area (SA) and subdivide nasal space are used as morphological proxies for olfactory and respiratory physiology. The present study offers additional details on the nasal fossa of the adult mouse lemur (Microcebus murinus), previously described by Smith and Rossie (Smith and Rossie [2008]; Anatomical Record 291:895-915). Additional, intervening histological sections of the specimen were used to map and quantify the distribution of olfactory and nonolfactory mucosa on the smaller turbinal of the frontal recess (FR; frontoturbinal) and those that occur between ethmoturbinals (ETs; interturbinals). A second adult Microcebus specimen, available as a dried skull, was scanned using microcomputed tomography (microCT) and reconstructed to infer the position of these turbinals within the nasal airway. Overall, turbinal bones comprise more than half of internal nasal SA. All ETs combined comprise about 30% of total nasal fossa SA, and contribute nearly half of all olfactory SA. Of these, the nasoturbinal (NT) is most completely covered with olfactory mucosa, whereas ET I is least covered with olfactory mucosa. The FR contributes significantly to total olfactory SA (ca. 20%). This recess and the single frontoturbinal within it lie in a more lateral pathway of airflow compared with interturbinals, which lie in more central zone just anterior to the olfactory recess of Microcebus. Variations in the turbinals and recesses that complicate central and paranasal in primates should be investigated further in light of zone-specific distributions of olfactory receptors (ORs) that differ between these regions in rodents.

First direct evidence of hibernation in an eastern dwarf lemur species (Cheirogaleus crossleyi) from the high-altitude forest of Tsinjoarivo, central-eastern Madagascar.

The nocturnal dwarf lemurs of Madagascar (genus Cheirogaleus) are the only primates known to be obligate hibernators. Although the physiology of hibernation has been studied widely in the western, small-bodied species, Cheirogaleus medius, no direct evidence of hibernation, i.e., body temperature recordings, has been reported for any of the three recognized eastern dwarf lemur species. We present skin temperature data collected by external collar transmitters from two eastern dwarf lemur individuals (Cheirogaleus crossleyi) captured in the high-altitude forest of Tsinjoarivo, central-eastern Madagascar. Our study species is larger in body size than western dwarf lemurs and inhabits much colder environments. We present the first evidence of hibernation in an eastern dwarf lemur species, and we compare the results with data available for the western species. Although the hibernation period is shorter in dwarf lemurs from Tsinjoarivo, minimum body temperatures are lower than those reported for C. medius. Both individuals at Tsinjoarivo showed limited passive and extended deep hibernation during which they did not track ambient temperature as observed in most western dwarf lemurs. Because ambient temperatures at Tsinjoarivo never exceed 30°C, dwarf lemurs have to experience arousals to maintain homeostasis during periods of hibernation. We show that large dwarf lemurs (>400 g) are capable of undergoing deep hibernation and suggest that cold, high-altitude forests may render hibernation highly advantageous during periods of food scarcity. This study has implications for understanding the physiology of hibernation in small-bodied lemurs.