Large Comparative Analyses of Primate Body Site Microbiomes Indicate that the Oral Microbiome Is Unique among All Body Sites and Conserved among Nonhuman Primates.

The study of the mammalian microbiome serves as a critical tool for understanding host-microbial diversity and coevolution and the impact of bacterial communities on host health. While studies of specific microbial systems (e.g., in the human gut) have rapidly increased, large knowledge gaps remain, hindering our understanding of the determinants and levels of variation in microbiomes across multiple body sites and host species. Here, we compare microbiome community compositions from eight distinct body sites among 17 phylogenetically diverse species of nonhuman primates (NHPs), representing the largest comparative study of microbial diversity across primate host species and body sites. Analysis of 898 samples predominantly acquired in the wild demonstrated that oral microbiomes were unique in their clustering, with distinctive divergence from all other body site microbiomes. In contrast, all other body site microbiomes clustered principally by host species and differentiated by body site within host species. These results highlight two key findings: (i) the oral microbiome is unique compared to all other body site microbiomes and conserved among diverse nonhuman primates, despite their considerable dietary and phylogenetic differences, and (ii) assessments of the determinants of host-microbial diversity are relative to the level of the comparison (i.e., intra-/inter-body site, -host species, and -individual), emphasizing the need for broader comparative microbial analyses across diverse hosts to further elucidate host-microbial dynamics, evolutionary and biological patterns of variation, and implications for human-microbial coevolution. IMPORTANCE The microbiome is critical to host health and disease, but much remains unknown about the determinants, levels, and evolution of host-microbial diversity. The relationship between hosts and their associated microbes is complex. Most studies to date have focused on the gut microbiome; however, large gaps remain in our understanding of host-microbial diversity, coevolution, and levels of variation in microbiomes across multiple body sites and host species. To better understand the patterns of variation and evolutionary context of host-microbial communities, we conducted one of the largest comparative studies to date, which indicated that the oral microbiome was distinct from the microbiomes of all other body sites and convergent across host species, suggesting conserved niche specialization within the Primates order. We also show the importance of host species differences in shaping the microbiome within specific body sites. This large, comparative study contributes valuable information on key patterns of variation among hosts and body sites, with implications for understanding host-microbial dynamics and human-microbial coevolution.

Cryptic diversity and species boundaries within the Paragalago zanzibaricus species complex.

The recently described genus Paragalago is a complex of several nocturnal and morphologically cryptic species distributed in the forests of eastern Africa. Species diversity within this genus has been mainly described using species-specific differences in their loud calls. However, molecular data are still lacking for this group and species boundaries remain unclear. In this study, we explore species diversity within the zanzibaricus-complex using a combination of mitochondrial and nuclear data and comparing multiple species delimitation methods. Our results consistently support the existence of three independent lineages, P. cocos, P. zanzibaricus, and P. granti, confirming previous hypotheses based on vocal data. We conclude that these three lineages represent valid cryptic species and we hypothesize that speciation within this complex was characterized by cycles of forest expansion and contraction in the Plio-Pleistocene.

Species Boundaries within Morphologically Cryptic Galagos: Evidence from Acoustic and Genetic Data.

Describing primate biodiversity is one of the main goals in primatology. Species are the fundamental unit of study in phylogeny, behaviour, ecology and conservation. Identifying species boundaries is particularly challenging for nocturnal taxa where only subtle morphological variation is present. Traditionally, vocal signals have been used to identify species within nocturnal primates: species-specific signals often play a critical role in mate recognition, and they can restrict gene flow with other species. However, little research has been conducted to test whether different "acoustic forms" also represent genetically distinct species. Here, we investigate species boundaries between two putative highly cryptic species of Eastern dwarf galagos (Paragalago cocosand P. zanzibaricus). We combined vocal and genetic data: molecular data included the complete mitochondrial cytochrome b gene (1,140 bp) for 50 samples across 11 localities in Kenya and Tanzania, while vocal data comprised 221 vocalisations recorded across 8 localities. Acoustic analyses showed a high level of correct assignation to the putative species (approx. 90%), while genetic analyses identified two separate clades at the mitochondrial level. We conclude that P. cocos and P. zanzibaricus represent two valid cryptic species that probably underwent speciation in the Late Pliocene while fragmented in isolated populations in the eastern forests.

Sleep patterns, daytime predation, and the evolution of diurnal sleep site selection in lorisiforms.

OBJECTIVES: Synthesize information on sleep patterns, sleep site use, and daytime predation at sleep sites in lorisiforms of Asia and Africa (10 genera, 36 species), and infer patterns of evolution of sleep site selection. MATERIALS AND METHODS: We conducted fieldwork in 12 African and six Asian countries, collecting data on sleep sites, timing of sleep and predation during daytime. We obtained additional information from literature and through correspondence. Using a phylogenetic approach, we established ancestral states of sleep site selection in lorisiforms and traced their evolution. RESULTS: The ancestral lorisiform was a fur-clinger and used dense tangles and branches/forks as sleep sites. Use of tree holes and nests as sleep sites emerged ∼22 Mya (range 17-26 Mya) in Africa, and use of bamboo emerged ∼11 (7-14) Mya in Asia and later in Africa. Fur clinging and some sleep sites (e.g., tree holes, nests, but not bamboo or dense tangles) show strong phylogenetic signal. Nests are used by Galagoides, Paragalago, Galago and Otolemur; tree holes by Galago, Paragalago, Sciurocheirus and Perodicticus; tangles by Nycticebus, Loris, Galagoides, Galago, Euoticus, Otolemur, Perodicticus and Arctocebus; all but Sciurocheirus and Otolemur additionally sleep on branches/forks. Daytime predation may affect sleep site selection and sleep patterns in some species of Nycticebus, Galago, Galagoides, Otolemur and Perodicticus. Most lorisiforms enter their sleep sites around sunrise and leave around sunset; several are active during twilight or, briefly, during daytime. CONCLUSION: Variations in sleep behavior, sleep patterns and vulnerability to daytime predation provide a window into the variation that was present in sleep in early primates. Overall, lorisiforms use the daytime for sleeping and no species can be classified as cathemeral or polycyclic.

A giant among dwarfs: a new species of galago (Primates: Galagidae) from Angola.

OBJECTIVES: Based on vocalization recordings of an unknown galago species, our main objectives were to compare morphology and call structure with known closely-related taxa and describe a new species of galago. MATERIALS AND METHODS: We conducted field surveys in three forest habitats along the escarpment region in western Angola (Kumbira Forest, Bimbe Area, and Northern Scarp Forest), and examined galago specimens from museums worldwide. We digitized and analyzed calls using Avisoft SASLab Pro software. We also compared museum specimens from Angola with other Galago and Galagoides specimens, and conducted comparative analyses (ANOVA and between group principle component analysis) based on a set of twelve linear measurements of skulls and teeth. RESULTS: We describe the new species to which we give the name Angolan dwarf galago, Galagoides kumbirensis sp. nov. The new species has a loud and characteristic crescendo call, used by other Galagoides spp. (sensu stricto) in West Africa to attract companions and repel rivals. However, this call shows species-typical differences from its closest relatives. Galagoides kumbirensis sp. nov. is also distinguished by differences in the skull morphology, pelage color and facial markings, as well as a larger body size, similar to that of Galago moholi, which is not known to be sympatric. CONCLUSION: This discovery points to the importance of Angolan forests as refuges for endemic biodiversity. These forests are under severe threat from overexploitation, and there is an urgent need to establish conservation measures and designate protected areas.

Remarkable ancient divergences amongst neglected lorisiform primates.

Lorisiform primates (Primates: Strepsirrhini: Lorisiformes) represent almost 10% of the living primate species and are widely distributed in sub-Saharan Africa and South/South-East Asia; however, their taxonomy, evolutionary history, and biogeography are still poorly understood. In this study we report the largest molecular phylogeny in terms of the number of represented taxa. We sequenced the complete mitochondrial cytochrome b gene for 86 lorisiform specimens, including ∼80% of all the species currently recognized. Our results support the monophyly of the Galagidae, but a common ancestry of the Lorisinae and Perodicticinae (family Lorisidae) was not recovered. These three lineages have early origins, with the Galagidae and the Lorisinae diverging in the Oligocene at about 30 Mya and the Perodicticinae emerging in the early Miocene. Our mitochondrial phylogeny agrees with recent studies based on nuclear data, and supports Euoticus as the oldest galagid lineage and the polyphyletic status of Galagoides. Moreover, we have elucidated phylogenetic relationships for several species never included before in a molecular phylogeny. The results obtained in this study suggest that lorisiform diversity remains substantially underestimated and that previously unnoticed cryptic diversity might be present within many lineages, thus urgently requiring a comprehensive taxonomic revision of this primate group.

The primates of the Udzungwa Mountains: diversity, ecology and conservation.

The Udzungwa Mountains are one of the most important areas in Africa for primate diversity and conservation, with two endemic monkeys (Udzungwa red colobus Procolobus gordonorum and Sanje mangabey Cercocebus [galeritus] sanjei), and the near-endemic kipunji monkey Rungwecebus kipunji, a new genus and species discovered in 2004 and found in Udzungwa and Southern Highlands. With six species of galagos, or bushbabies, the area is also of exceptional importance for nocturnal primates. The form of Mountain galago Galagoides orinus occurring in the Udzungwa Mountains appears to be distinct on the base of vocalizations, and further work will be required to assess its taxonomic status. The primate community reflects the overall, exceptional biodiversity of these isolated and ancient mountains. The Udzungwa are part of the Eastern Arc mountain chain, a centre of global importance for biodiversity and endemism. Of all the Eastern Arc Mountain blocks, the Udzungwa have the largest forested area, widest altitudinal gradient and greatest habitat diversity. We review current knowledge on the diversity and distribution of the primate community of the Udzungwa Mountains, with an emphasis on ecology and conservation.

Comparative penile morphology of East African galagos of the genus Galagoides (family Galagidae): implications for taxonomy.

Recent studies on the comparative penile morphology of galagos have revealed complex patterns that vary among both genera and species, and help with species identification. So far the penile morphologies of 14 galago species have been described and an identification key has been proposed. The present study extends and revises previous work. Wild Galagoides cocos, G. granti, G. zanzibaricus and G. rondoensis from the Eastern Arc Mountains and coastal forests of Tanzania and Kenya were live-trapped, and one species (G. orinus) was examined using a museum specimen. Penile morphology was photographed, traced, and described qualitatively. All of the mature males had penile spines. Spines were absent or indistinct in immature males of all of the species. The penile morphologies of G. cocos, G. granti, and G. zanzibaricus are similar in their overall distribution and type of spines, but differ in the shape of the glans penis. Both G. orinus and G. rondoensis have divergent penile morphologies compared to all other galagos, and are probably phylogenetically distinct. The results support other recent morphological and behavioral studies that consider these five galagos to be distinct species. The evolution of the baculum and spines is thought to be linked to sexual selection in multimale mating systems, but the mechanisms involved are not entirely understood. Adult male G. rondoensis appear to display the penile spines by exposing the distal section of the penis.

Species-typical patterns of infant contact, sleeping site use and social cohesion among nocturnal primates in Africa.

This paper provides a checklist and summary of what is currently known of the variation in infant contact, sleeping site preference and aspects of social cohesion in the nocturnal primates of Africa. Genera and species are compared, based on previously unpublished field observations and a review of the literature. There is a clear pattern of similarity between the species within each genus and distinct differences between genera. Species in the same genus tend to be ecologically equivalent and replace each other allopatrically, whereas species in different genera are more likely to be sympatric, with up to 6 species living together. Maximum sympatry within genera is found in Otolemur and Galagoides, where species are ecologically divergent. This may reflect an ancient origin of species within these genera or suggest that further taxonomic revision is required at the generic level. Some data are recorded for the first time for species that have only recently been separated (cryptic species), but some taxa remain very poorly known. It is concluded that field studies are still at an elementary stage and further research with radio tracking is urgently needed in the face of rapidly declining habitats.