Population and genetic structure of a male-dispersing strepsirrhine, Galago moholi (Primates, Galagidae), from northern South Africa, inferred from mitochondrial DNA.

The habitats of Galago moholi are suspected to be largely fragmented, while the species is thought to be expanding further into the southernmost fringe of its range, as well as into human settlements. To date, no intraspecific molecular genetic studies have been published on G. moholi. Here we estimate the genetic diversity and connectivity of populations of G. moholi using two mitochondrial gene regions, the cytochrome C oxidase subunit I gene (COI) and the displacement loop of the control region (D-loop). Samples from five localities in northern South Africa were obtained from archived collections. The two mitochondrial DNA gene regions were amplified and sequenced to provide population summary statistics, differentiation [proportion of the total genetic variation in a population relative to the total genetic variance of all the populations (FST), differentiation within populations among regions (ΦST)], genetic distance and structure. There was discernible genetic structure among the individuals, with two COI and six D-loop haplotypes belonging to two genetically different groups. There was population differentiation among regions (FST = 0.670; ΦST = 0.783; P < 0.01). However, there were low levels of differentiation among populations, as haplotypes were shared between distant populations. Adjacent populations were as divergent from each other as from distant populations. The results suggest that genetic introgression, most likely due to past migrations or recent unintentional translocations that include the animal trade, may have led to connectivity among populations.

A digital collection of rare and endangered lemurs and other primates from the Duke Lemur Center.

Scientific study of lemurs, a group of primates found only on Madagascar, is crucial for understanding primate evolution. Unfortunately, lemurs are among the most endangered animals in the world, so there is a strong impetus to maximize as much scientific data as possible from available physical specimens. MicroCT scanning efforts at Duke University have resulted in scans of more than 100 strepsirrhine cadavers representing 18 species from the Duke Lemur Center. An error study of the microCT scanner recovered less than 0.3% error at multiple resolution levels. Scans include specimen overviews and focused, high-resolution selections of complex anatomical regions (e.g., cranium, hands, feet). Scans have been uploaded to MorphoSource, an online digital repository for 3D data. As captive (but free ranging) individuals, these specimens have a wealth of associated information that is largely unavailable for wild populations, including detailed life history data. This digital collection maximizes the information obtained from rare and endangered animals with minimal degradation of the original specimens.

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.

Low Geographic and Subspecific Variation in the Loud Call of the Widespread and Phenotypically Cryptic Northern Lesser Galago (Galago senegalensis) Suggests Taxonomic Uniformity.

Like other nocturnal primates, many species of galago (Galagidae) are phenotypically cryptic, making their taxonomic status difficult to resolve. Recent taxonomic work has disentangled some of the confusion. This has resulted in an increase in the number of recognised galago species. The most widespread galago species, and indeed the most widespread nocturnal primate, is the northern lesser galago (Galago senegalensis) whose geographic range stretches >7,000 km across Africa. Based on morphology, 4 subspecies are currently recognised: G. s. senegalensis, G. s. braccatus, G. s. sotikae and G. s. dunni. We explore geographic and subspecific acoustic variation in G. senegalensis, testing three hypotheses: isolation by distance, genetic basis, and isolation by barrier. There is statistical support for isolation by distance for 2 of 4 call parameters (fundamental frequency and unit length). Geographic distance explains a moderate amount of the acoustic variation. Discriminant function analysis provides some degree of separation of geographic regions and subspecies, but the percentage of misdesignation is high. Despite having (putative) parapatric geographic ranges, the most pronounced acoustic differences are between G. s. senegalensis and G. s. dunni. The findings suggest that the Eastern Rift Valley and Niger River are significant barriers for G. senegalensis. The acoustic structures of the loud calls of 121 individuals from 28 widespread sites are not significantly different. Although this makes it unlikely that additional unrecognised species occur within G. senegalensis at the sites sampled, vast areas of the geographic range remain unsampled. We show that wide-ranging species do not necessarily exhibit large amounts of variation in their vocal repertoire. This pattern may also be present in nocturnal primates with smaller geographic ranges.

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.

Identification of a new genomic hot spot of evolutionary diversification of protein function.

Establishment of phylogenetic relationships remains a challenging task because it is based on computational analysis of genomic hot spots that display species-specific sequence variations. Here, we identify a species-specific thymine-to-guanine sequence variation in the Glrb gene which gives rise to species-specific splice donor sites in the Glrb genes of mouse and bushbaby. The resulting splice insert in the receptor for the inhibitory neurotransmitter glycine (GlyR) conveys synaptic receptor clustering and specific association with a particular synaptic plasticity-related splice variant of the postsynaptic scaffold protein gephyrin. This study identifies a new genomic hot spot which contributes to phylogenetic diversification of protein function and advances our understanding of phylogenetic relationships.

Allometry and evolution in the galago skull.

To probe the ontogenetic bases of morphological diversity across galagos, we performed the first clade-wide analyses of growth allometries in 564 adult and non-adult crania from 12 galagid taxa. In addition to evaluating if variation in galago skull form results from the differential extension/truncation of common ontogenetic patterns, scaling trajectories were employed as a criterion of subtraction to identify putative morphological adaptations in the feeding complex. A pervasive pattern of ontogenetic scaling is observed for facial dimensions across galagids, with 2 genera also sharing relative growth trajectories for masticatory proportions (Galago, Galagoides). As the facial growth series and adult data are largely coincidental, interspecific variation may result from character displacement and consequent selection for size differentiation among sister taxa. Derived configurations of the jaw joint and jaw muscle mechanical advantage in Otolemur and Euoticus appear to facilitate increased gape during scraping behaviors. Differences in aspects of masticatory growth and form characterizing these 2 genera highlight selection to uncouple shared ontogenetic patterns, which occurred via transpositions that retained ancestral scaling patterns. Due to the lack of increased robusticity of load-resisting mandibular elements in Otolemur and Euoticus, there is little evidence to suggest that exudativory in galagos results in correspondingly higher masticatory stresses.

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.

Brief communication: histology and micro CT as methods for assessment of facial suture patency.

The extent of fusion in facial sutures has implications for topics ranging from biomechanics to phylogeny reconstruction. An unfortunate limitation of studying sutural fusion in skeletal specimens is that it is difficult to assess whether apparently patent sutures are in fact fused internally. Both histology and microcomputed tomography (CT) are potential tools for solving this, but relatively few studies have attempted to discern the limits of micro CT for visualization of microanatomical structures. We examined microanatomical aspects of facial sutures in adult cadaveric samples from captive bushbabies. Premaxillary and nasopremaxillary sutures were examined in serially sectioned snouts of four greater bushbabies (Otolemur garnettii) and four lesser bushbabies (Galago moholi). Sections containing sutures with osseous bridging were rated as "fused," and the presence or absence of grooves on the external side was recorded. One bushbaby was studied using micro CT prior to physical sectioning. O. garnettii and two of the G. moholi show multiple foci of fusion. Histological examination confirmed that sutural fusion is limited to the internal surface in numerous sections, resulting in an external notch. Such points of internal fusion could be clearly visualized in raw CT slices. The presence of such notches suggests that external examination can underestimate the degree of suture fusion. Thus, microanatomical evidence may be needed to fully assess biomechanical correlates and phylogenetic interpretations based on fusion of facial sutures. Our results also indicate micro CT may be a useful tool to obtain this evidence.

Fossil evidence for an ancient divergence of lorises and galagos.

Morphological, molecular, and biogeographic data bearing on early primate evolution suggest that the clade containing extant (or 'crown') strepsirrhine primates (lemurs, lorises and galagos) arose in Afro-Arabia during the early Palaeogene, but over a century of palaeontological exploration on that landmass has failed to uncover any conclusive support for that hypothesis. Here we describe the first demonstrable crown strepsirrhines from the Afro-Arabian Palaeogene--a galagid and a possible lorisid from the late middle Eocene of Egypt, the latter of which provides the earliest fossil evidence for the distinctive strepsirrhine toothcomb. These discoveries approximately double the previous temporal range of undoubted lorisiforms and lend the first strong palaeontological support to the hypothesis of an ancient Afro-Arabian origin for crown Strepsirrhini and an Eocene divergence of extant lorisiform families.

Three acoustic forms of Allen's galagos (primates; Galagonidae) in the Central African region.

This study identifies populations currently classified as Allen's galago (Galago alleni) at ten locations in Gabon, Cameroon and Bioko Island. Morphological diversity was evident both within and between populations. Attention to the loud calls revealed three distinct vocal profiles which are consistent within biogeographical regions. This work is based on the Recognition Concept of Species which refers to a Specific Mate Recognition System. Galagos rely less on visual signals than diurnal primates and recognise each other principally by means of auditory and olfactory signals. Galagos possess repertoires of loud calls relating to contact and alarm which are thought to be species-specific. Other studies of nocturnal prosimians (galagos, tarsiers) have demonstrated that the unique loud call repertoires are reliable indicators of species boundaries; whereas characters such as body size and pelage coloration are highly variable, even within populations. The vocal data in this study provide evidence of at least three acoustic forms of galago within the Allen's group which are predicted to represent three distinct species: the Allen's form on Bioko Island and south-west Cameroon, the Gabon form in southern Cameroon and northern Gabon and the Makandé form in Gabon south of the Ogooué river. Some populations may be vulnerable to extinction due to limited distributions and habitat destruction.

Chromosome painting reveals that galagos have highly derived karyotypes.

The differences in chromosome number between Otolemur crassicaudatus (2n = 62) and Galago moholi (2n = 38) are dramatic. However, the total number of signals given by hybridizing human chromosome paints to galago metaphases is similar: 42 in O. crassicaudatus and 38 G. moholi. Many human chromosome homologs are found fragmented in each species, and numerous translocations have resulted in chromosomal syntenies or hybridization associations which differ from those found in humans. Only 7 human autosomes showed conserved synteny in O. crassicaudatus, and 9 in G. moholi. Both galago species have numerous associations or syntenies not found in humans: O. crassicaudatus has 11, and G. moholi has 21. The phylogenetic line leading to the last common ancestor of the two galago species accumulated 6 synapomorphic fissions and 5 synapomorphic fusions. Since the divergence of the two galago species, 10 Robertsonian translocations have further transformed the G. moholi karyotype, and 2 fissions have been incorporated into the O. crassicaudatus karyotype. Comparison with other primates, tree shrews, and other mammals shows that both galagos have karyotypes which are a mixture of derived and conserved chromosomes, and neither has a karyotype close to that of the proposed ancestor of all primates. Am J Phys Anthropol 117:319-326, 2002. Published 2002 Wiley-Liss, Inc.

Bushbaby growth hormone is much more similar to nonprimate growth hormones than to rhesus monkey and human growth hormones.

Unlike other mammals, Old World primates have five growth hormone-like genes that are highly divergent at the amino acid level from the single growth hormone genes found in nonprimates. Additionally, there is a change in the interaction of growth hormone with its receptor in humans such that human growth hormone functions in nonprimates, whereas nonprimate growth hormone is ineffective in humans. A Southern blotting analysis of the genome of a prosimian, Galago senegalensis, revealed a single growth hormone locus. This single gene was PCR-amplified from genomic DNA and sequenced. It has a rate of nonsynonymous nucleotide substitution less than one fourth that of the human growth hormone gene, while the rates of synonymous substitution in the two species are less different. Human and rhesus monkey growth hormones exhibit variation at a number of amino acid residues that can affect receptor binding. The galago growth hormone is conservative at each of these sites, indicating that this growth hormone is functionally like nonprimate growth hormones. These observations indicate that the amplification and rapid divergence of primate growth hormones occurred after the separation of the higher primate lineage from the galago lineage.

New species of bushbaby from the middle Miocene of Maboko Island, Kenya.

A mandible recovered from ca. 15 million year old deposits of Maboko Island, Kenya, represents the first bushbaby known from the middle Miocene. The specimen is from a new species of Komba, a genus previously known from early Miocene occurrences in western Kenya and northeastern Uganda. Komba is revised, with emended diagnoses proposed for the genus, type-species, and referred species. Komba sp. nov. is distinguished by its larger size and differences of molar cusp acuity, buccal cingulum expression, and mental foramen configuration. Contrary to previous opinion, species of Komba probably diverged prior to the last common ancestor of extant Galaginae, and it is unlikely that they represent early stages of living bushbaby species lineages. Although contemporary Progalago is widely regarded as a galagine, aspects of upper molar, lower premolar, and mandibular corpus morphology indicate that it is more closely related to lorisines. Unlike the greater success currently enjoyed by bushbabies, lorisines were more diverse and almost as abundant as galagines in the early Miocene of eastern Africa.

Variations in vocal patterns of Senegal and South African lesser bushbabies and their implications for taxonomic relationships.

Vocalizations of Senegal and South African lesser bushbabies were compared with respect to their acoustic properties analysed from spectrograms and oscillograms. Homologous calls could be identified within comparable functional categories. Considerable similarities were revealed in most of the noisy vocalizations associated with aggressive, defensive or anxiety and alarm behaviour. Striking divergences were detected, however, in almost all of the tonal or harmonic call types given in association with contact or contact-seeking, defensive or alarm behaviour. The results provide strong support for the separation of the two forms into distinct species, Galago senegalensis and Galago moholi.

Morphological clues to genetic species: multivariate analysis of greater Galago sibling species.

Several studies conducted in diverse fields indicate the presence of a genetic discontinuity within the taxon Galago crassicaudatus E. Geoffroy--the thick-tailed bushbaby. One of these areas is morphology. This contribution details a statistical analysis of skull material classified under this taxon in order 1) to confirm the objective existence of two morphotypes, and 2) to investigate the characters that allow the skull types to be distinguished. Emphasis is placed on multivariate techniques, although univariate and bivariate techniques are included where they are felt to be appropriate. All statistical analyses point to the reality of the morphological discontinuity between the groups. This is true even when size considerations have been reduced by rescaling the data. The results support separation of the populations at a specific level: G. crassicaudatus and G. garnettii. In addition, the structural changes observed in the two taxa--including an increase in overall size in G. crassicaudatus--are indicative of a divergence in preferred habitats: G. garnettii is adapted to more mesic environmental conditions, and to a softer, less fibrous diet than is its more robust sibling.