Infant survival and litter size in primigravid and multigravid Galagos

Eighteen years of birth records for three species of Galago at the Duke University Primate Center were examined to determine the effect of gravidity status on neonatal mortality and litter size. Multiparous Galago senegalensis moholi and G crassicaudatus, but not G garnettii, had significantly higher infant survival rates. Gravidity status had no effect on the percentage of multiple births for any of the three species of Galago.     

Reproductive and dietary parameters in wild greater galago populations

Information concerning habitat, body size, reproductive status, and diet was recorded from 348 greater galagos, captured at six different localities in Tanzania and southern Africa between 1953 and 1955. The localities extended from Pemba Island in the north to Chikwawa, Malawi, in the south and varied broadly in the same order in degree of climatic aridity— from well-watered clove and coconut plantations to seasonally very dry woodland. Animals from the three northern localities fell within the geographic range of Galago garnettii,while the rest were assumed to be G. crassicaudatus.Statistical analysis of body size parameters confirmed this allocation. Data on fetal occurrence, vaginal and labial condition, and lactation indicate a restricted breeding season for both species, with peak proportions in estrus in August in G. garnettiiand in May-July in G. crassicaudatus.Gut content data indicate a variety of foods, with a preponderance in the northern localities of soft fruit such as mango, pawpaw, and coconut pulp; gum was a major carbohydrate source in the southernmost localities. Contrary to expectations, tooth damage, in the form of both loss and breakage, was much more prevalent in G. garnettiithan in G. crassicaudatus.The teeth most commonly lost were the upper incisors— perhaps because of the high acid and sugar content of a frugivorous diet. The high incidence of breakage of the lower incisors and upper canines indicates the inclusion of hard-shelled food sources in the diet of G. garnettii.     

Hematology, serum chemistry values, and rectal temperatures of adult greater galagos (Galago garnetti and G. crassicaudatus)

Hematological and serum chemistry values, as well as rectal temperatures, were obtained from greater galagos (Galago garnettii and G. crassicaudatus), in order to establish normative values. No species or sex differences were found for four hematological parameters and 15 serum chemistry parameters. Species differences were seen in phosphate, magnesium, cholesterol, alkaline phosphate, G-glutamyl transferase, mean corpuscular volume and leucocyte, neutrophil, and lymphocyte number. Significant sex differences were observed in glucose, hemoglobin, and hematocrit values. Species and sex differences were seen in chloride and erythrocyte number.     

Three-dimensional analysis of mandibular morphology in Otolemur

Euclidean distance matrix analysis (EDMA) of three-dimensional data is used here to examine mandibular morphology between two species of galagos. Otolemur crassicaudatus consumes primarily exudates, while O. garnettii is more frugivorous. Acquisition of exudates involves either gouging or scraping tree bark, and may involve different forces at the mandible than incising fruits. Previous studies of mandibular morphology in exudate-feeding primates produced mixed results, some suggesting that morphological specializations reflect adaptations for greater force at the anterior dentition, while others suggest specializations for producing a large gape. This study addresses these controversies by testing predictions associated with O. crassicaudatus generating greater force at the anterior dentition or producing a larger gape relative to O. garnettii. In addition, this study tests predictions associated with specializations of the anterior dentition in O. crassicaudatus as related to exudate-feeding. Crania and mandibles from 28 O. crassicaudatus and 17 O. garnettii were digitized in three dimensions, using 18 landmarks that summarize the shape of the jaw. Two-dimensional measurements were taken to assess incisor robusticity. All three-dimensional data were analyzed using EDMA, and bootstrap tests were executed to identify specific interlandmark differences that were driving any significant (P < 0.05) overall shape differences. Two-dimensional data were analyzed using Student's t-test for independent measures. Results revealed that there was a significant shape difference in mandibles between species, and that mandibles of O. crassicaudatus showed higher condyles, longer mandibles, decreased incisor procumbency, and greater incisor robusticity relative to O. garnettii. It is suggested that the results of the present study reflect adaptations for scraping in O. crassicaudatus rather than gouging.     

Histomorphology of the mandibular condylar cartilage in greater galagos (Otolemur spp.)

The functional morphology of the primate craniomandibular complex and temporomandibular joint (TMJ) components is frequently discussed in terms of gross skeletal structure. At the histomorphologic level, however, the TMJ has only been studied in Old World anthropoids. The present study is designed to describe the microanatomy of the condylar cartilage of the TMJ in two closely related species of greater galago: the exudativorous Otolemur crassicaudatus and the frugivorous O. garnettii. TMJs with intact joint capsules were harvested from adult, cadaveric specimens of these species (four O. crassicaudatus and five O. garnettii). The samples were decalcified, processed for paraffin sectioning, and sectioned at 10-18 microm in the coronal plane. The samples were then stained with hematoxylin/eosin, Gomori trichrome, and Alcian blue, and examined with a photomicroscope. Generally, condylar cartilage in O. crassicaudatus was thickest both laterally and centrally, while O. garnettii had the relatively thickest cartilage laterally. Both species displayed a superficial articular zone, a middle proliferative zone, and a deeply located hypertrophic zone in the condylar cartilage. O. crassicaudatus typically had the greatest cell density in each of these zones. In addition, O. crassicaudatus had focal concentrations of Alcian blue laterally and centrally, while O. garnettii had the greatest reactivity in the central portion only. These results suggest that O. crassicaudatus may be specialized to resist greater compressive force at the TMJ condylar cartilage in specific regions of the mandibular condyle.     

Morphological Correlates of Speciation in Bush Babies

Morphology is not a reliable specific indicator in nocturnal animals. Nevertheless, because species are genetically independent, appropriate analytic methods should reveal subtle and consistent morphological differences among them. Until recently, the diversity of living bush babies was underrated, and new species have been recognized on the basis of genetic, behavioral and soft tissue data. This has placed museum curators in a quandary as to how to sort their skin and skull collections according to the new specific designations.We conducted multivariate analyses of 6 morphologically similar pairs of bush baby taxa: Otolemur crassicaudatus and O. garnettii; Galagoides demidoffand G. thomasi; Galago gallarumand G. senegalensis; G. moholi and G. senegalensis; Euoticus elegantulus and E. pallidus, and Galagoides zanzibaricus and G. granti. We also compared subspecies within the taxa Otolemur crassicaudatus, O. garnettii, Galagoides demidoff, and Galago senegalensis. Five out of six species pairs were discriminated with a high level of reliability (88.5–99%) on the basis of 2–5 morphological variables. Only Euoticus elegantulus and E. pallidus did not show this pattern. All strongly supported specific discriminations share two features: (a) ear length is a highly significant factor, while the involvement of other characters is variable; (b) the greater the reliability of the discrimination, the fewer variables necessary to effect it. Euoticus elegantulus and E. pallidus behaved more like subspecies in the discrimination, while Galago senegalensis sspp. showed a pattern of variation similar to that in the specific analyses.     

Seasonal variation in the diet of South African Galagos

The feeding behavior and diet of two species of bushbaby, Galago senegalensisand Galago crassicaudatus,in South Africa were examined in relation to seasonal changes in climate. The populations studied were allopatric, but both fed predominantly on Acaciagum and invertebrates. Data on their diet were collected by direct observation of a radiocollared female of each species and by analysis of fecal samples. Differences in diet were found between the species within seasons and within species between the seasons. Both spent more time gum-feeding in winter than in summer. Prey size and type differed between the species in summer but converged in winter. The quantity of insects taken was fairly similar between seasons for G. senegalensisbut dropped considerably for G. crassicaudatusin winter. These observations are interpreted in terms of interspecific differences in feeding strategies, which are considered to be a function of the difference in body size of the two galago species.     

Comparative studies of morphology and reproduction in two subspecies of the Greater bushbaby, Galago crassicaudatus crassicaudatus and G. c. argentatus

Two subspecies of the Greater bushbaby, Galago crassicaudatus argentatus and G. c. crassicaudatus , are known to differ morphologically, but quantitative studies of the differences, or of reproductive compatability between the subspecies, have not previously been attempted. Somatic measurements were made on living specimens of both subspecies and controlled experiments were conducted to determine whether fertile matings would occur between them.
G. c. argentatus is heavier than G. c. crassicaudatus and has longer ears, a longer ulna and fibula and a greater biorbital breadth. A significant degree of sexual dimorphism in body weight and length of the fibula and ulna occurs in G. c. argentatus , males being larger than females. In G. c. crassicaudatus however, there are no statistical differences between the sexes in these somatic measurements. The morphology of the male and female external genitalia differs between the two subspecies.
In six pairs of male argentatus and female crassicaudatus , only one pair mated and no offspring resulted. In seven pairs of female argentatus and male crassicaudatus , matings occurred in all pairs but only one female conceived and this pregnancy ended prematurely in a spontaneous abortion. In control experiments using six oppositely-sexed pairs of G. c. crassicaudatus , however, all females became pregnant and produced live offspring.
The morphological and reproductive differences between G. c. argentatus and G. c. crassicaudatus are more pronounced than previously realized and it is possible that the two varieties may merit separation as distinct species of Galago.     

Unexpected Conservation of the X-Linked Color Vision Gene in Nocturnal Prosimians: Evidence from Two Bush Babies

Bush babies have had a long history of nocturnal life and it would be interesting to know whether their color vision genes have become degenerate. Therefore, we used PCR techniques to sequence the X-linked pigment gene of two of these nocturnal prosimians: Galago senegalensis and Otolemur garnettii. Southern hybridization of genomic DNA of G. senegalensis showed a single X-linked pigment gene. Interestingly, the deduced pigment sequences of the two bush babies are identical. By comparing the X-linked pigments of bush baby, human, squirrel monkey, and marmoset, 38 variable positions were identified. At those positions that may cause a spectral shift, the bush baby pigment has identical or biochemically similar residues to those of the marmoset cone pigment with a spectral peak of 543 nm. This result is consistent with the estimate of 544–545 nm for the spectral peak of the X-linked pigment of Otolemur crassicaudatus, which is closely related to Otolemur garnettii. The neighbor-joining tree of mammalian X-linked pigments showed a significantly shorter branch in the bush baby lineage than in other primate lineages. A relative rate test showed that the nonsynonymous substitution rate of the bush baby X-linked pigment gene is about three times slower than that of the human red pigment gene, though the synonymous substitution rates of the two genes are similar. The slower nonsynonymous rate in the bush baby lineage suggests that the bush baby X-linked pigment gene is under functional constraints, in spite of its nocturnal life. Two radical changes at positions in the intradiskal surface next to the sixth transmembrane domain were observed in the X-linked cone pigment of bush babies but not in other primates. They are changes from Ala to Ser and from Asn to His, which are similar in function to the corresponding residues in rhodopsins. These two changes may be of importance for dim light sensitivity, which is consistent with our proposal that the evolution of the bush baby X-linked pigment gene is under selective pressure. In addition, the 2.5% divergence in introns 2 and 5 of the X-linked pigment gene between the two bush babies supports their classification into two separate genera. Received: 30 November 1996 / Accepted: 17 June 1997     

Scaling of growth and life history traits relative to body size, brain size, and metabolic rate in lorises and galagos (Lorisidae, primates)

A broad range of variation in body size, brain size, and metabolic rate occurs within the primate family Lorisidae, thus providing an opportunity to examine the relationship of these three parameters to variation in growth and life history traits. Data on adult body weight, gestation length, lactation length, age at first estrus, litter size, and growth parameters were collected from a captive colony of four lorisid species, Loris tardigradus, Nycticebus coucang, Galago crassicaudatus, and G. senegalensis. The data presented here constitute the most complete life history information available for these poorly understood prosimian species. Correlation and allometric analyses were performed to determine the relationships between variables. Among the lorisids studied, adult body weight, adult cranial capacity, and relative cranial capacity did not predict variation in life history traits. Adult basal metabolic rate predicted most of the variability in gestation length, lactation length, and growth parameters. Lorisines differ from similarly sized galagines in having lower basal metabolic rates, slower growth rates, slower developmental rates, and smaller litter sizes, resulting in reduced reproductive potential. This may be a consequence of lorisine adaptation to a diet of toxic insects. Metabolic rate and diet may be among the most important parameters to examine in any study of life history evolution.     

Reproductive patterns in galagos (Galago zanzibaricus and Galago garnettii) in relation to climatic variability

The reproductive patterns (birth seasonality, litter size, litters per year) of two sympatric species of galago (Galago zanzibaricus and G. garnettii) were studied in a coastal forest in Kenya for a two-year period. Trap-retrap and radio tracking methods were employed. G. zanzibaricus has one infant twice per year; G. garnettii has one infant once per year. Both species are seasonal breeders. These East African galagos are intermediate in reproductive patterns when compared with galagos from South African woodland (G. senegalensis moholi and G. crassicaudatus umbrosis) and West African rainforest (G. alleni and G. demidovii). Climatic patterns (total annual rainfall, seasonal variability of rainfall, variability in total annual rainfall, and annual temperature variability) are also compared for the three regions. Climatically, East Africa is intermediate between West and South Africa in total annual rainfall and in seasonality of rainfall, but not in year-to-year variability in rainfall. East Africa shows the highest variability in annual rainfall. South Africa has the coldest dry seasons and highest variability in temperatures. The results of this study suggest that “r-selection” and “K-selection” do not provide adequate explanations of galago reproductive patterns.     

Static intraspecific allometry of the dentition in Otoletnur crassicaudatus

Adult static intraspecific allometry of tooth size was evaluated in a sample of 66 Otolemur crassicaudatus (34 male, 32 female). Tooth areas were calculated from mesiodistal and buccolingual measurements of canines and postcanine teeth of both arcades and were scaled to four viscerocranial measurements: bimaxillary width; maxillo-alveolar length; mandibular length and bigonial width. Individual tooth crown areas were also scaled to total skull length, body length and body weight. From the log-transformed analyses it is concluded that postcanine tooth size was unrelated to body length or weight, and poorly correlated to skull length or jaw size. Although viscerocranial size appears to be independent of body size, these measures are well correlated to skull length. It is shown that the longer the skull, the shorter and narrower the maxilla, and the longer and broader the mandible. Canines are shown to scale negatively allometric to skull length, hence, large animals will have relatively small canines.     

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.     

Distribution of erythrocytic allozymes in two sibling species of greater galago [Galago crassicaudatus E. Geoffroy 1812 and G. garnettii (Ogilby 1838)]

This study investigated the use of erythrocyte enzymes as indicators of the presence or absence of gene flow between the sibling species G. crassicaudatus and G. garnettii. Fifty-five animals deriving from 14 different source populations were included in the analyses. In addition to hemoglobin, eight enzyme systems were examined: acid phosphatase, adenylate kinase, carbonic anhydrase II, esterase D, glucose-6-phosphate dehydrogenase, 6-phosphogluconate dehydrogenase, peptidase A, and peptidase B. of these, adenylate kinase, glucose-6-phosphate dehydrogenase, hemoglobin, peptidase A, and peptidase B showed no interspecific or intraspecific variation. Esterase D was polymorphic in certain populations of G. crassicaudatus but not in others or in G. garnettii. Acid phosphatase and 6-phosphogluconate dehydrogenase were polymorphic in G. garnettii but monomorphic in all G. crassicaudatus populations. The taxa showed fixation for different alleles at the carbonic anhydrase II locus, indicating a lack of gene exchange between the taxa. We suggest that acid phosphatase, 6-phosphogluconate dehydrogenase, and carbonic anhydrase II may be used as genetic markers in the identification of these two taxa.     

Speciation in the greater galagos (Prosimii: Galaginae): review and synthesis*

A marked morphological and genetical discontinuity among the greater galagos points to the existence of two genetical species within the taxon, Galago crassicaudatus E. Geofl'roy 1812. This contribution investigates the conditions surrounding this speciation event, and places it within a phylogenetic context. Information pertaining to body size, litter size, sexual dimorphism, locomotor mode and karyotypic structure is assessed. It is hypothesized that G. crassicaudatus diverged from its more gracile sibling, G. garnettii, approximately 2 million years ago, in respotise lo the increasing aridification of Africa that accompanied the Northern Hemisphere Pleistocene glaciations.     

Loud calls ofGalago crassicaudatus andG. garnettii and their relation to habitat structure

Long distance vocalizations have been shown to be good indicators of genetic species in primates. Here the loud calls of two recently identified greater galago taxa —Galago crassicaudatus andG. garnettii — are compared and analyzed statistically. Observed differences in call structures are investigated further as potential indicators of differences in the structures of habitats frequented by the two species. Although the calls share a repetitive structure, and show similar dominant frequency bands (1,000 – 1,500 Hz), they differ significantly in the number of units per call, unit duration, inter-unit interval, highest frequency, lowest frequency, dominant frequency band, first harmonic, and call duration. The duration of theG. crassicaudatus call is more than twice that ofG. garnettii. Strong intraspecific consistency is seen in the most energetic frequency bands (dominant frequency band and first harmonic), and durations of the individual units and inter-unit intervals. Information important to species recognition is thus most likely to be contained in these features. Individual recognition may be encoded in the relative emphasis of higher level harmonics. The frequency structures of the calls will reflect requirements for acoustical transmission in a forest environment, as well as structural constraints imposed by body size. Higher frequencies detected in theG. garnettii call (up to 8,500 Hz) may have a functional significance related to distance estimation, or may simply be a reflection of smaller body size. The greater modulation of theG. garnettii call suggests that its habitat constitutes a denser or more turbulent medium for sound transmission than does the habitat ofG. crassicaudatus.     

Primate red cell enzymes: glucose-6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase

Glucose-6-phosphate dehydrogenase (E. C.: 1.1.1.49) phenotypes and 6-phosphogluconate dehydrogenase (E. C.: 1.1.1.44) phenotypes were determined by starch-gel electrophoresis of red cell hemolysates of Galago crassicaudatus subspp., Propithecus verreauxi, Lemur spp., Hapalemur griseus, and Macaca mulatta. A single glucose-6-phosphate dehydrogenase (G6PD) phenotype was found in each species. A single 6-phosphogluconate dehydrogenase (6PGD) phenotype was found in Lemur spp., Hapalemur griseus, and Galago crassicaudatus argentatus. In a group of six Propithecus verreauxi, three 6PGD phenotypes, PGD A, PGD AB, and PGD B, were found. Three phenotypes, PGD A, PGD AB, and PGD B, were found in 38 G. c. crassicaudatus. The three phenotypes in each species are apparently the products of two codominant autosomal alleles, PGD^A and PGD^B. The frequency of PGD^A in G. c. crassicaudatus is 0.263. A population of 260 free-ranging macaques displays a polymorphism at the 6PGD locus. Three phenotypes, PGD A, PGD AB, and PGD B, were found. These also appear to be controlled by two codominant autosomal alleles, PGD^A and PGD^B the frequency of PGD^A = 0.913. Additional analysis of three well-defined troops within the macaque population indicated that there are no significant differences between the troops or within the population at the 6PGD locus.     

Mitochondrial Sequences as Indicators of Genetic Classification in Bush Babies

Systematic relationships among the African bush babies are not well understood. Various generic designations are currently in use. Some authors refer all species to a single genus (Galago), while others recognize 4 genera. Phylogenetic reconstructions based on morphology, karyology, allozymes and vocal repertoires have generated inconsistent hypotheses of relationship. We analyzed partial sequences of three mitochondrial genes (270 bp from cytochrome b, 387 bp from 12S rRNA, and 241 bp from 16S rRNA, total 898 bp) to resolve some uncertainties. We sampled taxa from each of three genera: Galagoides alleni, G. demidoff and G. zanzibaricus; Galago senegalensis, G. gallarum and G. moholi; and Otolemur crassicaudatus and O. garnettii. Outgroup taxa were Asian lorises: Nycticebus coucang and Loris tardigradus. We analyzed sequences separately and in combination, and modeled phylogenies using maximum parsimony, weighted parsimony, neighbor-joining and maximum-likelihood. We obtained some variation in phylogenetic inference depending on sequence and analytical method, but the results also gave strong phylogenetic signals. The lesser bush babies invariably formed a clade, showing evidence of very recent radiation. The greater bush babies also formed a clade, marked by somewhat greater interspecific genetic distances, which was allied with Galagoides alleni in most instances. Galagoides demidoff and G. zanzibaricus are not closely related, though both diverged early in the history of the group. A genus comprising Galagoides alleni, G. demidoff and G. zanzibaricus is not supported by our data. The most likely alliance for Galagoides alleni is within the genus Otolemur. Of the three partial sequences employed in the study, 16S rRNA gave the most consistent results, while cytochrome b was least informative.     

Patterns of sexual dimorphism in body weight among prosimian primates.

Many primatologists believe that there is no sexual dimorphism in body size in prosimian primates. Because this belief is based upon data that came from only a few species and were largely flawed in some aspect of sample quality, I re-examined the extent of sexual dimorphism in body weight, using weights of 791 adult prosimians from 34 taxa recorded over the last 17 years at the Duke University Primate Center. There was no significant sex difference in body weight in 17 species, but males were significantly larger in Nycticebus pygmaeus, Tarsius syrichta, Galago moholi, Galagoides demidovii, Otolemur crassicaudatus and Otolemur garnettii. Moreover, females were significantly larger in Microcebus murinus. Thus, the general lack of sexual dimorphism could be confirmed, notably for lemurs, but prosimians as a group show more variability in sexual size dimorphism than was previously thought. After including previously published data obtained in the wild from 8 additional species, I found significant heterogeneity in the degree of sexual dimorphism at the family level, but only the Indridae and Galagidae were significantly different from each other. Among the prosimian infraorders, the Lorisiformes were significantly more dimorphic than the Lemuriformes. Differences in dimorphism between higher taxonomic groups are discussed in the context of prosimian evolution, concluding that phylogenetic inertia cannot provide a causal explanation for the evolution of sexual dimorphism. The relative monomorphism of most prosimians may be related to allometric constraints and, especially in the Lemuriformes, to selective forces affecting male and female behavioral strategies.     

GEOMETRIC MORPHOMETRICS OF THE SKULL ROOF OF STEREOSPONDYLS (AMPHIBIA: TEMNOSPONDYLI)

Abstract:  Geometric morphometric analysis using relative warps is applied to the skull roof of 62 species of stereospondyls and their closest outgroups (i.e. basal archegosauriforms) from among temnospondyl amphibians. Twenty-one landmarks and five taxonomic groups are used for comparisons. Their skull evolution is quantified in a morphospace defined by two relative warps axes. The majority of groups show poor concordance between morphological and phylogenetic distances. The only exception is represented by Yates and Warren's study of stereospondyl relationships, in which concordance is high. Only basal archegosauriforms and rhinesuchids show significant overlap in morphospace, although this might be due to low sample sizes. Regression of estimated mean disparity against taxon sample size shows that species within both the trematosauroid and the rhytidostean groups are more widely dispersed in morphospace than species belonging to any of the remaining stereospondyl groups. Stereospondyl skull evolution was characterized by divergence between major clades and convergence within those clades. Changes in patterns of morphospace occupation through time agree with the hypothesis of an 'explosive' radiation in the early Early Triassic, after the extinction of basal archegosauriforms at the end of the Permian.