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Concept: Strepsirrhini

168

Specialized acrobatic leaping has been recognized as a key adaptive trait tied to the origin and subsequent radiation of euprimates based on its observed frequency in extant primates and inferred frequency in extinct early euprimates. Hypothesized skeletal correlates include elongated tarsal elements, which would be expected to aid leaping by allowing for increased rates and durations of propulsive acceleration at takeoff. Alternatively, authors of a recent study argued that pronounced distal calcaneal elongation of euprimates (compared to other mammalian taxa) was related primarily to specialized pedal grasping. Testing for correlations between calcaneal elongation and leaping versus grasping is complicated by body size differences and associated allometric affects. We re-assess allometric constraints on, and the functional significance of, calcaneal elongation using phylogenetic comparative methods, and present an evolutionary hypothesis for the evolution of calcaneal elongation in primates using a Bayesian approach to ancestral state reconstruction (ASR). Results show that among all primates, logged ratios of distal calcaneal length to total calcaneal length are inversely correlated with logged body mass proxies derived from the area of the calcaneal facet for the cuboid. Results from phylogenetic ANOVA on residuals from this allometric line suggest that deviations are explained by degree of leaping specialization in prosimians, but not anthropoids. Results from ASR suggest that non-allometric increases in calcaneal elongation began in the primate stem lineage and continued independently in haplorhines and strepsirrhines. Anthropoid and lorisid lineages show stasis and decreasing elongation, respectively. Initial increases in calcaneal elongation in primate evolution may be related to either development of hallucal-grasping or a combination of grasping and more specialized leaping behaviors. As has been previously suggested, subsequent increases in calcaneal elongation are likely adaptations for more effective acrobatic leaping, highlighting the importance of this behavior in early euprimate evolution.

Concepts: Haplorrhini, Evolution, Primates, Tarsier, Evolutionary physiology, Strepsirrhini, Phylogenetic comparative methods, Primate

57

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.

Concepts: Haplorrhini, Simian, Fossil, Lemur, Bat, Strepsirrhini, Phylogenetics, Primate

52

While it is well known that the primate brain evolved to cope with complex social contingencies, the neurophysiological manifestation of social interactions in primates is not well understood. Here, concurrent wireless neuronal ensemble recordings from pairs of monkeys were conducted to measure interbrain cortical synchronization (ICS) during a whole-body navigation task that involved continuous social interaction of two monkeys. One monkey, the passenger, was carried in a robotic wheelchair to a food dispenser, while a second monkey, the observer, remained stationary, watching the passenger. The two monkeys alternated the passenger and the observer roles. Concurrent neuronal ensemble recordings from the monkeys' motor cortex and the premotor dorsal area revealed episodic occurrence of ICS with probability that depended on the wheelchair kinematics, the passenger-observer distance, and the passenger-food distance - the social-interaction factors previously described in behavioral studies. These results suggest that ICS represents specific aspects of primate social interactions.

Concepts: Strepsirrhini, Ape, Sociology, Monkey, Cerebral cortex, Brain, Simian, Primate

28

Among the Strepsirrhini, molar size does not exhibit a consistent dietary signal when body mass is used to size-adjust molar dimensions. This observation is also true for anthropoid primates, but when postcanine size is expressed relative to the size of the facial skeleton in this clade, folivorous anthropoids tend to have relatively larger postcanine teeth than anthropoids in other dietary categories. The contrast in the results generated by these two independent size variables appears to be related to systematic differences in facial size in the Anthropoidea, particularly between short-faced colobines and long-faced cercopithecines. The goal of this study was to determine whether a similar pattern of relationships characterizes strepsirrhines. Data on molar area, facial size, body mass, and diet for forty-three extant strepsirrhines and seven subfossil lemurs were analyzed using phylogenetic generalized least squares. Results indicate that strepsirrhine folivores tend to have larger molars than frugivores relative to the size of the facial skeleton. Insectivorous species exhibit a wide range of variation in relative molar size that appears to be taxonomically patterned: lorisids in this dietary category resemble folivores, whereas galagids resemble frugivores. These results confirm the generality of the anthropoid pattern and support the idea that, in some contexts, it may be useful to consider elements of the masticatory system relative to their functional and developmental environments rather than to overall organismal size. The biological significance of having large postcanine teeth relative to the size of the face, but not body mass, is discussed with reference to a model that identifies the size of the oral cavity as the most functionally relevant standard for assessing the relative size of the postcanine dentition.

Concepts: Aye-aye, Fossil, Simian, Teeth, Lemur, Ring-tailed Lemur, Strepsirrhini, Primate

24

Assessing manual lateralization in non-human primates could be an optimal way to understand the adaptive value of this asymmetry in humans. Though many studies have investigated hand preferences in Old and New World monkeys and apes, fewer studies have considered manual lateralization in strepsirrhines, especially in experimental tasks. This study investigated hand preferences for a unimanual and a bimanual task of 17 captive ring-tailed lemurs (Lemur catta), housed at Parco Natura Viva (VR), Italy. The effect of age on handedness has been also investigated. The lemurs were tested on a unimanual task, in which subjects were restricted to using one hand to retrieve the food inside an apparatus, and on a bimanual task, in which lemurs had to use one hand to keep the apparatus door open while reaching with the other hand to retrieve the food inside it. At the population-level, our results revealed an asymmetrical hand use distribution, in particular a bias toward a right hand preference for food reaching in both the unimanual and the bimanual tasks. Furthermore, at the individual-level, the bimanual task seems to elicit a greater hand preference than the unimanual task. Results of this study underline the importance of experimental tasks in determining hand preference in strepsirrhines. Furthermore, as bimanual tasks elicited a stronger degree of lateralization, they appear to be more suited to investigate manual laterality. Finally, findings from this study highlight the presence of a right hand preference in ring-tailed lemurs, shedding new light on the evolution of human right handedness. Am. J. Primatol. © 2016 Wiley Periodicals, Inc.

Concepts: Left-handedness, Right-handedness, Handedness, Lemuridae, Lemur, Strepsirrhini, Ring-tailed Lemur, Primate

17

The fossil record of early primates is largely comprised of dentitions. While teeth can indicate phylogenetic relationships and dietary preferences, they say little about hypotheses pertaining to the positional behavior or substrate preference of the ancestral crown primate. Here we report the discovery of a talus bone of the dentally primitive fossil euprimate Donrussellia provincialis. Our comparisons and analyses indicate that this talus is more primitive than that of other euprimates. It lacks features exclusive to strepsirrhines, like a large medial tibial facet and a sloping fibular facet. It also lacks the medially positioned flexor-fibularis groove of extant haplorhines. In these respects, the talus of D. provincialis comes surprisingly close to that of the pen-tailed treeshrew, Ptilocercus lowii, and extinct plesiadapiforms for which tali are known. However, it differs from P. lowii and is more like other early euprimates in exhibiting an expanded posterior trochlear shelf and deep talar body. In overall form, the bone approximates more leaping reliant euprimates. The phylogenetically basal signal from the new fossil is confirmed with cladistic analyses of two different character matrices, which place D. provincialis as the most basal strepsirrhine when the new tarsal data are included. Interpreting our results in the context of other recent discoveries, we conclude that the lineage leading to the ancestral euprimate had already become somewhat leaping specialized, while certain specializations for the small branch niche came after crown primates began to radiate.

Concepts: Lemur, Pen-tailed Treeshrew, Phylogenetic tree, Cladistics, Strepsirrhini, Phylogenetics, Treeshrew, Primate

14

Lemurs are the most threatened group of mammals on earth. Lemur catta (ring-tailed lemur) represents one of the most iconic lemur species and faces numerous anthropogenic threats in the wild. In this study, we present population estimates from 32 sites across the range of L. catta, collected from primary and secondary data sources, to assess the number of ring-tailed lemurs left in the wild. We estimate that there are approximately 2,220 individual L. catta remaining in the 32 sites considered. We note local extinctions of populations of L. catta in at least 12 of the 32 sites examined, and that significantly more extinctions occurred in areas without some form of protection. This decrease in extant populations could represent a decrease of more than 95% of all ring-tailed lemurs in Madagascar since the year 2000. While these results should be considered preliminary, we stress the rapid decline of the species and note that habitat loss, bushmeat hunting and the illegal pet trade are driving populations to local extinction. Based on the data presented here, urgent and immediate funding and conservation action are crucial to ensure the viability of the remaining wild populations of ring-tailed lemurs.

Concepts: Strepsirrhini, Endangered species, Conservation biology, Primate, Madagascar, Lemur, Ring-tailed Lemur, Extinction

5

The oldest primates of modern aspect (euprimates) appear abruptly on the Holarctic continents during a brief episode of global warming known as the Paleocene-Eocene Thermal Maximum, at the beginning of the Eocene (∼56 Ma). When they first appear in the fossil record, they are already divided into two distinct clades, Adapoidea (basal members of Strepsirrhini, which includes extant lemurs, lorises, and bushbabies) and Omomyidae (basal Haplorhini, which comprises living tarsiers, monkeys, and apes). Both groups have recently been discovered in the early Eocene Cambay Shale Formation of Vastan lignite mine, Gujarat, India, where they are known mainly from teeth and jaws. The Vastan fossils are dated at ∼54.5 Myr based on associated dinoflagellates and isotope stratigraphy. Here, we describe new, exquisitely preserved limb bones of these Indian primates that reveal more primitive postcranial characteristics than have been previously documented for either clade, and differences between them are so minor that in many cases we cannot be certain to which group they belong. Nevertheless, the small distinctions observed in some elements foreshadow postcranial traits that distinguish the groups by the middle Eocene, suggesting that the Vastan primates-though slightly younger than the oldest known euprimates-may represent the most primitive known remnants of the divergence between the two great primate clades.

Concepts: Simian, Lorisidae, Omomyid, Lemur, Haplorrhini, Eocene, Strepsirrhini, Primate

4

Broca’s area in the ventrolateral prefrontal cortex (vlPFC) has a crucial role in human volitional speech production; damage to this area causes severe impairment of speech production. Lesions in PFC of monkeys, however, have only mild effects on spontaneous vocal behaviour. Non-human primate vocalizations are thus believed to constitute affective utterances processed by a subcortical network. Here in contrast to this assumption, we show that rhesus monkeys can control their vocalizations in a goal-directed way. During single-cell recordings in the vlPFC of monkeys trained to vocalize in response to visual cues, we find call-related neurons that specifically predict the preparation of instructed vocalizations. The activity of many call-related neurons before vocal output correlates with call parameters of instructed vocalizations. These findings suggest a cardinal role of the monkey homologue of Broca’s area in vocal planning and call initiation, a putative phylogenetic precursor in non-human primates for speech control in linguistic humans.

Concepts: Ape, Monkey, Strepsirrhini, Rhesus Macaque, Simian, Brain, Human, Primate

3

Interspecific variation in facial color patterns across New and Old World primates has been linked to species recognition and group size. Because group size has opposite effects on interspecific variation in facial color patterns in these two radiations, a study of the third large primate radiation may shed light on convergences and divergences in this context. We therefore compiled published social and ecological data and analyzed facial photographs of 65 lemur species to categorize variation in hair length, hair and skin coloration as well as color brightness. Phylogenetically controlled analyses revealed that group size and the number of sympatric species did not influence the evolution of facial color complexity in lemurs. Climatic factors, however, influenced facial color complexity, pigmentation and hair length in a few facial regions. Hair length in two facial regions was also correlated with group size and may facilitate individual recognition. Since phylogenetic signals were moderate to high for most models, genetic drift may have also played a role in the evolution of facial color patterns of lemurs. In conclusion, social factors seem to have played only a subordinate role in the evolution of facial color complexity in lemurs, and, more generally, group size appears to have no systematic functional effect on facial color complexity across all primates.

Concepts: Strepsirrhini, Phylogenetic tree, Phylogenetics, Speciation, Biology, Primate, Evolution, Lemur