Elevational Ranges of Lemurs in the Humid Forests of Madagascar

The geological history of Madagascar contains events that may have given rise to unusual factors that molded the primate communities of the island. In order to understand the impact of the factors we reviewed the elevational distribution of extant primate species in the humid forests. The elevational structuring of primates in the humid forests of Madagascar shows considerable differences from other tropical areas in the New World and Asia, which is correlated with the lack of large tracts of humid lowland habitat on Madagascar since it split from India.     

Possible Fruit Protein Effects on Primate Communities in Madagascar and the Neotropics

Background

The ecological factors contributing to the evolution of tropical vertebrate communities are still poorly understood. Primate communities of the tropical Americas have fewer folivorous but more frugivorous genera than tropical regions of the Old World and especially many more frugivorous genera than Madagascar. Reasons for this phenomenon are largely unexplored. We developed the hypothesis that Neotropical fruits have higher protein concentrations than fruits from Madagascar and that the higher representation of frugivorous genera in the Neotropics is linked to high protein concentrations in fruits. Low fruit protein concentrations in Madagascar would restrict the evolution of frugivores in Malagasy communities.

Methodology/Principal Findings

We reviewed the literature for nitrogen concentrations in fruits from the Neotropics and from Madagascar, and analyzed fruits from an additional six sites in the Neotropics and six sites in Madagascar. Fruits from the Neotropical sites contain significantly more nitrogen than fruits from the Madagascar sites. Nitrogen concentrations in New World fruits are above the concentrations to satisfy nitrogen requirements of primates, while they are at the lower end or below the concentrations to cover primate protein needs in Madagascar.

Conclusions/Significance

Fruits at most sites in the Neotropics contain enough protein to satisfy the protein needs of primates. Thus, selection pressure to develop new adaptations for foods that are difficult to digest (such as leaves) may have been lower in the Neotropics than in Madagascar. The low nitrogen concentrations in fruits from Madagascar may contribute to the almost complete absence of frugivorous primate species on this island.     

The evolution of nonhuman primate loud calls: Acoustic adaptation for long-distance transmission

Many nonhuman primates produce species-typical loud calls used to communicate between and within groups over long distances. Given their observed spacing functions, primate loud calls are likely to show acoustic adaptations to increase their propagation over distance. Here we evaluate the hypothesis that primates emit loud calls at relatively low sound frequencies to minimize their attenuation. We tested this hypothesis within and between species. First, we compared the frequencies of loud calls produced by each species with those of other calls from their vocal repertoires. Second, we investigated the relationship between loud call frequency and home range size across a sample of primate species. Comparisons indicated that primates produce loud calls at lower frequencies than other calls within their vocal repertoires. In addition, a significant negative relationship exists between loud call frequency and home range size among species. The relationship between call frequency and range size holds after controlling for the potentially confounding effects of body size and phylogeny. These results are consistent with the hypothesis that nonhuman primates produce loud calls at relatively low frequencies to facilitate their transmission over long distances.     

The Narrow Niche hypothesis: gray squirrels shed new light on primate origins

Current hypotheses for primate origins propose that nails and primate-like grasping hands and feet were important early adaptations for feeding in fine branches. Comparative research in this area has focused on instances of convergence in extant animals, showing that species with primate-like morphology feed predominantly from terminal branches. Little has been done to test whether animals without primate-like morphology engage in similar behavior. We tested the fine-branch niche hypothesis for primate origins by observing branch use in Eastern gray squirrels, Sciurus carolinensis, a species lacking primate grasping adaptations that has been understudied in the context of primate origins. We hypothesized that because gray squirrels lack primate-like grasping adaptations, they would avoid feeding and foraging in terminal branches. Instantaneous focal animal sampling was used to examine the locomotor and postural behaviors used while feeding and foraging. Our results demonstrate habitual and effective usage of terminal branches by gray squirrels while feeding and foraging, primarily on tree seeds (e.g., oak, maple, and elm). Discriminant function analysis indicates that gray squirrels feed and forage like primates, unlike some other tree squirrel species. Given the absence of primate-like features in gray squirrels, we suggest that although selection for fine-branch foraging may be a necessary condition for primate origins, it is not sufficient. We propose an alternative model of primate origins. The Narrow Niche hypothesis suggests that the primate morphological suite evolved not only from selection pressure for fine branch use, but also from a lack of engagement in other activities.     

Plasma testosterone transport in primates

All primate species, including Old and New World primates and prosimians have a plasma testosterone-estradiol binding globulin (TeBG), which is a glycoprotein and has a similar mobility in polyacrylamide gel electrophoresis. In New World primates the TeBG binding capacity for [3H]testosterone was higher and its affinity lower than in Old World primates. These changes were associated with high unbound plasma testosterone concentrations in these species. Binding parameters of TeBG in prosimian species varied markedly. Thus, in primate evolution TeBG was conserved despite marked differences in binding characteristics. In New World primates changes are associated with high total and unbound testosterone, a finding concordant with alterations of other steroid hormones concentration in these species with "generalized steroid hormone resistance".     

The Social Systems of Gregarious Lemurs: Lack of Convergence with Anthropoids due to Evolutionary Disequilibrium?

The gregarious lemurs of Madagascar show a lack of convergence with anthropoid primates in several social, demographic, morphological and ecological features. They lack sexual dimorphism in canine and body size, and live in groups with equal adult sex ratios that can vary in composition from pairs to larger units. In most species, females dominate males, and have brief and often synchronized estruses. Finally, lemurs are often active during both day and night (i.e. cathemeral). Three hypotheses for this lack of convergence are discussed. The traditional explanation is that Madagascar's unique ecological pressures have forced females to exclude males from access to limiting resources, selecting for the other unique features as means to maintain female dominance over males. This idea is not logically consistent and is also poorly supported empirically. The second hypothesis claims that cathemerality imposes unique constraints on lemur social organization. The social behavior of cathemeral taxa is largely consistent with this idea. However, the social organization of the diurnal species is not. The third hypothesis claims that recent ecological changes, in particular the demise of large diurnal raptors, have produced a mismatch between current activity periods and adaptations to activity period. This idea is supported by a review of morphological adaptations to light conditions among lemurs, and, more generally, by a comparative analysis of cathemerality among tropical forest mammals. We conclude that the social systems of non-nocturnal lemurs are best considered as groups formed by species adapted to live in pairs. However, we cannot conclusively exclude the possibility that cathemeral activity is an old and stable activity pattern among lemurs. We indicate which data would decide the issue, and discuss the implications for views of social evolution of lemurs and other animals.     

Morphometry and allometry of the primate humerus

The primate distal humerus has been used both in phylogenetic reconstruction and in assessing locomotor and postural adaptations. This study uses an allometric approach to predict locomotor patterns of extant primates regardless of phylogenetic position. By showing the relationship between form and function in living primate taxa it will be possible to use this data set to predict locomotor behavior of extinct primates. Several linear measurements were taken from the distal humerus of 71 extant primate species (anthropoids and prosimians). Allometric regressions of each measurement were performed with mandibular M₂ area as a surrogate for body size. These measurements were used to determine if significant differences in distal humerus morphology exist among locomotor groups. The results were then used to test several hypotheses about the relationship between humeral form and function. For example, the hypothesis that suspensory primates have a large medial epicondyle is confirmed; the hypothesis that terrestrial quadrupeds have a deep olecranon fossa could not be confirmed with quantitative data. In addition to this hypothesis testing, the residuals from the allometric regressions of the humeral measurements were used in a discriminant functions analysis to estimate locomotor behavior from distal humerus morphology. The discriminant functions analysis correctly reclassified 64/71 (90%) species.     

Characterization of Circulating Natural Killer Cells in Neotropical Primates

Despite extensive use of nonhuman primates as models for infectious diseases and reproductive biology, imprecise phenotypic and functional definitions exist for natural killer (NK) cells. This deficit is particularly significant in the burgeoning use of small, less expensive New World primate species. Using polychromatic flow cytometry, we identified peripheral blood NK cells as CD3-negative and expressing a cluster of cell surface molecules characteristic of NK cells (i.e., NKG2A, NKp46, NKp30) in three New World primate species – common marmosets, cotton-top tamarins, and squirrel monkeys. We then assessed subset distribution using the classical NK markers, CD56 and CD16. In all species, similar to Old World primates, only a minor subset of NK cells was CD56+, and the dominant subset was CD56–CD16+. Interestingly, CD56+ NK cells were primarily cytokine-secreting cells, whereas CD56–CD16+ NK cells expressed significantly greater levels of intracellular perforin, suggesting these cells might have greater potential for cytotoxicity. New World primate species, like Old World primates, also had a minor CD56–CD16– NK cell subset that has no obvious counterpart in humans. Herein we present phenotypic profiles of New World primate NK cell subpopulations that are generally analogous to those found in humans. This conservation among species should support the further use of these species for biomedical research.     

The phylogenetic structure of primate communities: variation within and across continents

Aim Our goals are: (1) to examine the relative degree of phylogenetic overdispersion or clustering of species in communities relative to the entire species pool, (2) to test for across‐continent differences in community phylogenetic structure, and (3) to examine the relationship between species richness and community phylogenetic structure. Location Africa, Madagascar, Asia, and the Neotropics. Methods We collected species composition and phylogenetic data for over 100 primate communities. For each community, we calculated two measures of phylogenetic structure: (1) the net relatedness index (NRI), which provides a measure of the mean pairwise phylogenetic distance among all species in the community; and (2) the nearest taxon index (NTI), which measures the relative phylogenetic distance among the closest related species in a community. Both measures are relative to the phylogeny of the species in the entire species pool. The phylocom package uses a randomization procedure to test whether the NRI and NTI values are higher or lower than expected by chance alone. In addition, we used a Kruskal–Wallis test to examine differences in NRI and NTI across continents, and linear regressions to examine the relationship between species richness and NRI/NTI. Results We found that the majority of individual primate communities in Africa, Asia and the Neotropics consist of member species that are neither more nor less closely related than expected by chance alone. Yet 37% of Malagasy communities contain species that are more distantly related to each other compared with random species assemblages. Also, we found that the average degree of relatedness among species in communities differed significantly across continents, with African and Malagasy communities consisting of more distantly related taxa compared with communities in Asia and the Neotropics. Finally, we found a significant negative relationship between species richness and phylogenetic distance among species in African, Asian and Malagasy communities. The average relatedness among species in communities decreased as community size increased. Main conclusions The majority of individual primate communities exhibit a phylogenetic structure no different from random. Yet there are across‐continent differences in the phylogenetic structure of primate communities that probably result from the unique ecological and evolutionary characteristics exhibited by the endemic species found on each continent. In particular, the recent extinctions of numerous primates on Madagascar are likely responsible for the low levels of evolutionary relatedness among species in Malagasy communities.     

Signal convergence in fruits: a result of selection by frugivores?

The Dispersal Syndrome hypothesis remains contentious, stating that apparently nonrandom associations of fruit characteristics result from selection by seed dispersers. We examine a key assumption under this hypothesis, i.e. that fruit traits can be used as reliable signals by frugivores. We first test this assumption by looking at whether fruit colour allows birds and primates to distinguish between fruits commonly dispersed by birds or primates. Second, we test whether the colours of fruits dispersed by primates are more contrasting to primates than the colours of bird‐dispersed fruits, expected if fruit colour is an adaptation to facilitate the detection by seed dispersers. Third, we test whether fruit colour has converged in unrelated plant species dispersed by similar frugivores. We use vision models based on peak sensitivities of birds’ and primates’ cone cells. We base our analyses on the visual systems of two types of birds (violet and ultraviolet based) and three types of primates (trichromatic primates from the Old and the New Worlds, and a dichromatic New World monkey). Using a Discriminant Function Analysis, we find that all frugivore groups can reliably discriminate between bird‐ and primate‐dispersed fruits. Fruit colour can be a reliable signal to different seed dispersers. However, the colours of primate‐dispersed fruits are less contrasting to primates than those of bird‐dispersed fruits. Fruit colour convergence in unrelated plants is independent of phylogeny and can be better explained by disperser type, which supports the hypothesis that frugivores are important in fruit evolution. We discuss adaptive and nonadaptive hypotheses that can potentially explain the pattern we found.     

Adrenal 11-hydroxylase activity in a hypercortisolemic New World primate: adaptive intra-adrenal changes

The squirrel monkey, a representative New World primate, has high plasma cortisol and aldosterone concentrations when compared to Old World primates. We measured adrenal mitochondrial 11-hydroxylase (11-OHase) activity in squirrel monkeys and in two representative Old World species (cynomolgus and rhesus macaques) in an effort to explain these elevated plasma glucocorticoid and mineralocorticoid levels. The activity of 11-OHase was 5-fold higher in the squirrel monkey than in the Old World species tested. Calculated 11-OHase Vmax was different in the squirrel monkey and the cynomolgus. However, the Km values were similar in the New World primate when compared to cynomolgus. The ability of metyrapone to block 11-OHase was less in the former than in the latter. The data are consistent with the hypothesis that the squirrel monkey adrenal cortex possesses an increased number of 11-hydroxylase enzyme units compared to that of Old World primate species, and is therefore more efficient in producing cortisol. This difference in 11-OHase activity in the squirrel monkey, in addition to other previously reported adrenal steroidogenic enzyme alterations, may be adaptive in nature, favoring increased cortisol and aldosterone production in this and possibly other New World primate species.     

Are local patterns of anthropoid primate diversity related to patterns of diversity at a larger scale?

Aims (1) To determine the relationship between local and regional anthropoid primate species richness. (2) To establish the spatial and temporal scale at which the ultimate processes influencing patterns of primate species coexistence operate. Location Continental landmasses of Africa, South America and Asia (India to China, and all islands as far south as New Guinea). Methods The local–regional species richness relationship for anthropoid primates is estimated by regressing local richness against regional richness (independent variable). Local richness is estimated in small, replicate local assemblages sampled in regions that vary in total species richness. A strong linear relationship is taken as evidence that local assemblages are unsaturated and local richness results from proportional sampling of the regional pool. An asymptotic curvilinear relationship is interpreted to reflect saturated communities, where strong biotic interactions limit local richness and local processes structure the species assemblage. As a further test of the assumption of local assemblage saturation, we looked for density compensation in high‐density local primate assemblages. Results The local–regional species richness relationship was linear for Africa and South America, and the slope of the relationship did not differ between the two continents. For Asia, curvilinearity best described the relationship between local and regional richness. Asian primate assemblages appear to be saturated and this is confirmed by density compensation among Asian primates. However, density compensation was also observed among African primates. The apparent assemblage saturation in Asia is not a species–area phenomenon related to the small size of the isolated islands and their forest blocks, since similar low local species richness occurs in large forests on mainland and/or peninsular Asia. Main conclusions In Africa and South America local primate assemblage composition appears to reflect the influence of biogeographic processes operating on regional spatial scales and historical time scales. In Asia the composition of primate assemblages are by‐and‐large subject to ecological constraint operating over a relatively small spatial and temporal scale. The possible local influence of the El Niño Southern Oscillations on the evolution and selection of life‐history characteristics among Asian primates, and in determining local patterns of primate species coexistence, warrants closer inspection.     

Parallel evolution of a self-signal: humans and new world monkeys independently lost the cell surface sugar Neu5Gc

Human sialic acid biology is unusual and thought to be unique among mammals. Humans lack a functional cytidine monophosphate-N-acetylneuraminic acid hydroxylase (CMAH) protein and cannot synthesize the sugar Neu5Gc, an innate mammalian signal of self. Losing this sugar changed how humans interact with some of our deadliest pathogens: malaria, influenza, and streptococcus among others. We show that the New World monkeys, comprising the third of all primate species, have human-like sialic acid biology. They have lost Neu5Gc because of an independent CMAH inactivation ~30 million years ago (mya) (compared to ~3 mya in hominids). This parallel loss of Neu5Gc opens sialic acid biology to comparative phylogenetic analysis and reveals an unexpected conservation priority. New World monkeys risk infection by human pathogens that can recognize cells in the absence of Neu5Gc. This striking molecular convergence provides a mechanism that could explain the long-standing observation that New World monkeys are susceptible to some human diseases that cannot be transmitted to other primates.     

Incisor size and diet revisited: The view from a platyrrhine perspective

Allometric relationships between incisor size and body size were determined for 26 species of New World primates. While previous studies have suggested that the incisors of Old World primates, and anthropoids in general, scale isometrically with body size, the data presented here indicate a negative allometric relationship between incisor size and body size among New World species. This negative allometry was exhibited by platyrrhines when either upper or lower incisor row length was regressed against body weight, and when either least-squares or bivariate principal axis equations were used. When upper incisor length was plotted against skull length, negative allometry could be sustained using both statistical techniques only when the full sample of 26 species was plotted. The choice of variables to represent incisor size and body size, and the choice of a statistical technique to effect the allometric equation, had a more pronounced impact on the location of individual species with regard to lines of best fit. Platyrrhines as a group have smaller incisors relative to body size than do catarrhines, regardless of diet. Among New World primates, small incisors represent a plausible primitive condition; species with relatively large incisors manifest a phyletic change associated with a dietary shift to foods that require increased incisal preparation. The opposite trend characterizes Old World primates. In spite of the taxonomic differences in relative incisor size between platyrrhine and catarrhine primates, inferences about diet derived from an allometric equation for all anthropoids should prove reliable as long as the species with unknown diet does not lie at the upper end of the body size range for platyrrhines or catarrhines.     

The development of small primate models for aging research

Nonhuman primate (NHP) aging research has traditionally relied mainly on the rhesus macaque. But the long lifespan, low reproductive rate, and relatively large body size of macaques and related Old World monkeys make them less than ideal models for aging research. Manifold advantages would attend the use of smaller, more rapidly developing, shorter-lived NHP species in aging studies, not the least of which are lower cost and the ability to do shorter research projects. Arbitrarily defining "small" primates as those weighing less than 500 g, we assess small, relatively short-lived species among the prosimians and callitrichids for suitability as models for human aging research. Using the criteria of availability, knowledge about (and ease of) maintenance, the possibility of genetic manipulation (a hallmark of 21st century biology), and similarities to humans in the physiology of age-related changes, we suggest three species--two prosimians (Microcebus murinus and Galago senegalensis) and one New World monkey (Callithrix jacchus)--that deserve scrutiny for development as major NHP models for aging studies. We discuss one other New World monkey group, Cebus spp., that might also be an effective NHP model of aging as these species are longer-lived for their body size than any primate except humans.     

Prevalence of Epstein-Barr virus (EBV) antibodies in primate stocks of zoological gardens

Abstract: Examination of 387 serum samples from 41 primate species with two different ELISAs for the presence of IgG-antibodies against Epstein-Barr virus. Antibodies were detected in 15 out of 32 species of Old World primates and none in six species of New World primates by screening ELISA (Enzygnost, Behringwerke AG, Marburg), a testkit for human diagnostics. To avoid species-dependent factors which could influence the sensitivity of the Enzygnost assay, a competition ELISA was established. The modified test assessed antibodies in all species of Old World primates and three species of the New World primates.     

The role of tooth enamel mechanical properties in primate dietary adaptation

Primate teeth adapt to the physical properties of foods in a variety of ways including changes in occlusal morphology, enamel thickness, and overall size. We conducted a comparative study of extant primates to examine whether their teeth also adapt to foods through variation in the mechanical properties of the enamel. Nanoindentation techniques were used to map profiles of elastic modulus and hardness across tooth sections from the enamel-dentin junction to the outer enamel surface in a broad sample of primates including apes, Old World monkeys, New World monkeys, and lemurs. The measured data profiles feature considerable overlap among species, indicating a high degree of commonality in mechanical properties. These results suggest that differences in the load-bearing capacity of primate molar teeth are more a function of morphology-particularly tooth size and enamel thickness-than of underlying mechanical properties.     

Ecogeographic size variation in small-bodied subfossil primates from Ankilitelo, southwestern Madagascar

Variation in body size is well documented for both extant and extinct Malagasy primates, and appears to be correlated with geographic patterns of resource seasonality. Less attention has been paid to extant lemurs in subfossil collections, although it has been suggested that subfossil forms of extant species are characterized by greater size than their modern counterpart. This trend of phyletic size change has been related to climate change, habitat fragmentation, or human hunting. However, space- and time-averaging in the subfossil samples of previous studies may have obscured more general ecogeographic patterns underlying these size differences. Our objective is to examine size variation in subfossil still-extant primates within a regional comparative context to determine if subfossil and living forms conform to similar ecogeographic patterns. We report on the subfossil still-extant primate assemblage from Ankilitelo, southwestern Madagascar (approximately 500 yr BP) to test this hypothesis. The Ankilitelo primates were compared with museum specimens of known locality. Extant taxa were assigned to one of five distinct ecogeographic regions, including spiny thicket, dry deciduous forest, succulent woodland, lowland and subhumid rainforest. Comparisons of tooth size in extant lemurs reveal significant geographical patterns of variation within genera. In general, the primates from Ankilitelo are indeed larger than their modern counterpart. However, these differences fit an ecoregional model of size variation, whereby Ankilitelo species are comparable in size to living forms inhabiting ecoregions present near the cave today. This suggests that Malagasy primates have been subjected to similar patterns of resource seasonality for at least 500 years.     

Locomotor adaptations within the Cercopithecus Genus: a multivariate approach.

Multivariate analysis as a technique for investigating locomotor differentiation among primates has proven its power and usefulness in many studies on various skeletal dimensions. In these analyses primate genera were distributed and sometimes clustered in a manner that was interpretable based on current knowledge of gross locomotor differences. In an effort to advance our understanding of arboreality and terrestriality in primates, the present research involves a careful look for the most subtle morphological differences in locomotor behavior. It is believed that by looking at such subtle shape differences an understanding of what it means morphologically for a primate to be either more or less arboreal may be achieved. The species within the primate genus Cercopithecus were analyzed. This genus includes species which may be placed along a habitat (ground-living to tree-dwelling) or activity spectrum. The different habitats or activity patterns clearly require slight variations in patterns of movement, which in turn may require subtle structural adaptations. Multivariate analyses of 67 postcranial variables on seven species within the genus allowed detection of slight degrees of morphological variation. However, when morphological differences are small, size variance among specimens may take on an inflated importance. A substantial amount of work was devoted to finding the least biased method of removing size variance from the variables while incorporating a discrete size variable into the study. Using these transformed skeletal variables, interspecific groupings were discovered. Much of this infrastructure is then related to differing locomotor behavior and provides an insight into the fine structure of primate locomotor adaptation in an arboreal habitat.     

Evolution of the SEC1 gene in New World monkey lineages (Primates, Platyrrhini)

The structure and evolution of the SEC1 gene were examined for the first time in New World primates of the genera Alouatta, Aotus, Ateles, Brachyteles, Callicebus, Callithrix, Cebus, Chiropotes, Lagothrix, Leontopithecus, Pithecia, Saguinus, and Saimiri. This gene has a high CG content (63.8%) and an estimated heterogeneous size ranging from 795 (Callithrix) to 1041 bp (Pithecia), due to numerous indel events. Similar to other fucosyltransferases, three conserved regions are shared by these primates, except for the callitrichines, Aotus and Pithecia, in which indel events resulted in premature stop codons that are related to the production of a supposedly non-functional protein. Phylogenetic analysis of the SEC1 gene, transition/transversion rates, and nucleotide sequence alignment support the hypothesis that primate SEC1 evolved by divergent evolution, and that the lack of activity in some lineages occurred independently at least twice in New World primates, once in the Aotus-Cebus-Callitrichinae group and again in Pithecia. Likelihood-based inference of ancestral states for the activity of SEC1 leads us to suppose that inactivation of SEC1 in the Callitrichinae was a result of a more complex series of events than in Pithecia.