Milk composition reflects pattern of material care in prosimian primates

Hypothesized relationships between milk composition and life history traits were examined by analyzing mid-lactation milks of seven lemurs (Eulemur fulvus, E. macaco, E. rubriventer, E. mongoz, Varecia variegata, Hapalemur griseus, Lemur catta), three bushbabies (Otolemur crassicaudatus, O. garnettii, Galago moholi), and two lorises (Nycticebus coucang, Loris tardigradus); partial data were also obtained for the lemuroid Cheirogaleus medius. There were significant differences in milk composition among species within either Eulemur or Otolemur, but the four genera for which multiple samples were available (Eulemur, Varecia, Otolemur, and Nycticebus) exhibited large composition differences. Eulemur milk was, on average, very dilute (9.9% dry matter) and low in energy (0.49 kcal/g). These milks contained 0.9% fat, 1.2% protein, and 8.4% carbohydrate on a fresh weight basis. Protein energy comprised only about 15% of total milk energy. Varecia had significantly higher dry matter (13.5%), fat (3.2%), protein (4.2%), gross energy (0.80 kcal/g), and protein energy: total energy ratio (28%) than Eulemur. Milks of the lorisoid genera Otolemur and Nycticebus were very similar, and both had significantly higher dry matter (18.3, 16.3%), fat (7.6, 7.0%), and gross energy concentration (1.27, 1.13 kcal/g) than either lemuroid genus. Otolemur milk was higher in protein than Nycticebus milk. We conclude that lorises, bushbabies, and perhaps cheirogaleids produce relatively rich, energy-dense milks in comparison with anthropoid primates. However, dilute milks appear to be uniformly found among species of Eulemur and perhaps in Lemur catta. The milk of Varecia (and perhaps Hapalemur) is intermediate in composition. Differences in milk composition among prosimians may be related to differences in maternal care: prosimians that carry their young during lactation produce more dilute milks than do species which leave their young unattended for prolonged periods. When looking at primates as a whole, however, the picture is somewhat less clear, since the milks of some “parkers” like Varecia do closely resemble those of large anthropoid primates who carry their young. Am. J. Primatol. 41:195–211, 1997. © 1997 Wiley-Liss, Inc.     

New early Eocene anaptomorphine primate (Omomyidae) from the Washakie Basin,Wyoming, with comments on the phylogeny and paleobiology of anaptomorphines

Recent paleontological collecting in the Washakie Basin, southcentral Wyoming, has resulted in the recovery of over 100 specimens of omomyid primates from the lower Eocene Wasatch Formation. Much of what is known about anaptomorphine omomyids is based upon work in the Bighorn and Wind River Basins of Wyoming. This new sample documents greater taxonomic diversity of omomyids during the early Eocene and contributes to our understanding of the phylogeny and adaptations of some of these earliest North American primates. A new middle Wasatchian (Lysitean) anaptomorphine, Anemorhysis savagei, n. sp., is structurally intermediate between Teilhardina americana and other species of Anemorhysis and may be a sister group of other Anemorhysis and Trogolemur. Body size estimates for Anemorhysis, Tetonoides, Trogolemur, and Teilhardina americana indicate that these animals were extremely small, probably less than 50 grams. Analysis of relative shearing potential of lower molars of these taxa indicates that some were primarily insectivorous, some primarily frugivorous, and some may have been more mixed feeders. Anaptomorphines did not develop the extremes of molar specialization for frugivory or insectivory seen in extant prosimians. Incisor enlargement does not appear to be associated with specialization in either fruits or insects but may have been an adaptation for specialized grooming or food manipulation. © 1994 Wiley-Liss, Inc.     

Neocortical development and social structure in primates

The relationships between the relative size of the neocortex and differences in social structures were examined in prosimians and anthropoids. The relative size of the neocortex (RSN) of a given congeneric group in each superfamily of primates was measured based on the allometric relationships between neocortical volume and brain weight for each superfamily, to control phylogenetic affinity and the effects of brain size. In prosimians, “troop-making” congeneric groups (N=3) revealed a significantly larger RSN than solitary groups (N=6), and there was a significant, positive correlation between RSN and troop size. In the case of anthropoids, polygynous/frugivorous groups (N=5) revealed a significantly larger RSN than monogynous/frugivorous groups (N=8). Furthermore, a significant, positive correlation between RSN and troop size was found for frugivorous congeneric groups of the Ceboidea. These results suggest that neocortical development is associated with differences in social structure among primates.     

Meat eating and predation in captive-born semi-free-ranging Lemur fulvus and caged Lemur macaco

A group of brown lemurs, Lemur fulvus, and a group of black lemurs, Lemur macaco, at the Duke University Center for the Study of Primate Biology and History have been observed to capture and eat birds and lizards. Although vertebrate prey are not unusual for many carnivorous prosimians, folivorous prosimians never have been observed to take vertebrates in the wild and rarely even insects.     

Evolution of Metamorphism in Thymidylate Synthases Within the Primate Lineages

Crystal structures of human thymidylate synthase (hTS) revealed that the protein exists in active and inactive conformations, defined by the position of a loop containing the active site nucleophile. TS is highly homologous among diverse species; however, the residue at position 163 (hTS) differs among species. Arginine at this position is predicted by structural modeling to enable conformational switching. Arginine or lysine is reported at this position in all mammals in the GenBank and Ensembl databases, with arginine reported in only primates. Sequence analysis of the TS gene of representative primates revealed that arginine occurs at this relative position in all primates except a representative of prosimians. Mutant human proteins were created with residues at position 163 that occur in TSs from prokaryotes and eukaryotes. Catalytic constants (k _cat) of mutant enzymes were 45–149% of hTS, with the lysine mutant (R163K) exhibiting the highest k _cat. The effect of lysine substitution on solution structure and on ligand binding was investigated. R163K exhibited higher intrinsic fluorescence, a more negative molar ellipticity, and higher dissociation constants (K _d) for ligands that modulate protein conformation than hTS. Temperature effects on intrinsic fluorescence and catalytic activity of hTS and R163K are consistent with proteins populating different conformational states. The data indicate that the enzyme with arginine at the position corresponding to 163 (hTS) evolved after the divergence of prosimians and simians and that substitution of lysine by arginine confers unique structural and functional properties to the enzyme expressed in simian primates.     

Adult Male Scent-Marking in Lemur catta and Eulemur fulvus rufus

Scent-marking and olfactory communication are used extensively by prosimians and can provide spatial and temporal records of group movement and behavior. We compare rates of male scent-marking in relation to reproductive seasons, male dominance rank, and habitat use in two related prosimians: Lemur catta and Eulemur fulvus rufus. We collected scent-marking data on adult male Lemur catta at Beza-Mahafaly Reserve (dry forest), and on Eulemur fulvus rufus at Ranomafana National Park (rainforest), Madagascar. In Lemur, rates of overall scent-marking differed significantly by reproductive season, with higher rates occurring in mating and lactation/migration periods, whereas in Eulemur, reproductive season did not appear to affect scent-marking rates. Dominance rank of male Lemur catta did not affect rates of scent-marking. Among male Eulemur fulvus, dominance relations were not apparent; however, 2 of the 5 focal males scent-marked somewhat more frequently during the mating season and also experienced greater mating success. In Lemur catta, higher rates of scent-marking in the mating season may relate to indirect reproductive competition during a period of high aggression, while such mating competition was not as marked in Eulemur fulvus. Furthermore, higher rates of marking in resident male Lemur catta during male migration may correlate with vigilance toward immigrating males. Greater overall scent-marking rates in ring-tailed lemurs may relate to extensive intergroup home range overlap and no area of exclusive use, whereas the red-fronted lemur groups tended to forage in areas of their home range where little-to-no intergroup overlap occurred.     

The ecology of oligocene African anthropoidea

African anthropoids are first recorded in Early Oligocene deposits of the Fayum Province, Egypt. Six genera and nine species are recognized. Estimated body weights for these taxa are based on the regression equation log ₁₀(B) = 2.86log ₁₀(L) + 1.37, whereB is the bodyweight in grams, and Lis the M ₂ length in millimeters. The equation is derived from 106 species of living primates. Fayum species range in body weight from about 600 g (Apidium moustafai)to about 6000 g (Aegyptopithecus zeuxis).A similar range of body weight is found among extant Cebidae. The Fayum primates are larger than any extant insectivorous primates;this fact probably rules out a predominantly insectivorous diet. Extant frugivorous hominoids can be separated from folivorous hominoids on the basis of molar morphology. Folivorous apes (gorilla and siamang) have proportionately more shearing on their molars than do frugivorous species. Based on the hominoid analogy, the molar morphology of the Fayum species is consistent with a frugivorous diet. Parapithecus grangeristands apart from other Fayum species in having better developed molar shearing, possibly indicating that it had more fiber in its diet. Terrestrial species of Old World monkeys tend to have significantly higher molar crowns than do more arboreal species. This difference may relate to an increased amount of grit in the diet of the more terrestrial species, selecting for greater resistance to wear. Oligocene primates have molar crown heights consistent with a primarily arboreal mode of existence. However, the particularly high molar crowns of Parapithecus grangerisuggest that this species may have foraged on the ground to a considerable degree. Other evidence is advanced suggesting that Apidiummay have had a diurnal activity pattern.     

Dental topography of platyrrhines and prosimians: Convergence and contrasts

Dental topographic analysis is the quantitative assessment of shape of three‐dimensional models of tooth crowns and component features. Molar topographic curvature, relief, and complexity correlate with aspects of feeding behavior in certain living primates, and have been employed to investigate dietary ecology in extant and extinct primate species. This study investigates whether dental topography correlates with diet among a diverse sample of living platyrrhines, and compares platyrrhine topography with that of prosimians. We sampled 111 lower second molars of 11 platyrrhine genera and 121 of 20 prosimian genera. For each tooth we calculated Dirichlet normal energy (DNE), relief index (RFI), and orientation patch count (OPCR), quantifying surface curvature, relief, and complexity respectively. Shearing ratios and quotients were also measured. Statistical analyses partitioned effects of diet and taxon on topography in platyrrhines alone and relative to prosimians. Discriminant function analyses assessed predictive diet models. Results indicate that platyrrhine dental topography correlates to dietary preference, and platyrrhine‐only predictive models yield high rates of accuracy. The same is true for prosimians. Topographic variance is broadly similar among platyrrhines and prosimians. One exception is that platyrrhines display higher average relief and lower relief variance, possibly related to lower relative molar size and functional links between relief and tooth longevity distinct from curvature or complexity. Explicitly incorporating phylogenetic distance matrices into statistical analyses of the combined platyrrhine‐prosimian sample results in loss of significance of dietary effects for OPCR and SQ, while greatly increasing dietary significance of RFI. Am J Phys Anthropol 153:29–44, 2014. © 2013 Wiley Periodicals, Inc.     

Effects of inbreeding on infant mortality in captive primates

Breeding records for 16 primate colonies representing six families and both suborders were obtained from 10 institutions breeding primates in captivity and from the international studbook on one endangered species. Inbreeding coefficients relative to the founding population were calculated for each individual born. Individuals with an inbreeding coefficient of zero were classified as “noninbred” those with inbreeding coefficients greater than zero, as “inbred.” Infant mortality was defined as all deaths prior to the age of 6 months. Infant mortality of inbred young was higher than that of noninbred young in 15 of the 16 colonies surveyed (P =0.0003, one-tailed sign test). The higher mortality rate of the inbred young was significant by a Fisher’s exact test with a probability less than or equal to 0.05 in five of the individual colonies: Lemur fulvus, Saguinus fuscicollis illigeri, Saguinus fuscicollis, Leontopithecus rosalia,and Mandrillus sphinx.     

Primate immunoglobulin heavy chain constant gamma genes: an hypothesis of their evolution

Four Immunoglobulin gamma heavy chain isotypes are present in humans; the true phylogenetic relationship between the genes are not known because of the complex concerted evolution of the Ig multigene locus. Here we present data obtained from Southern blot analysis of the gamma genes in several primate species including prosimians (Lemur catta), New World Monkeys (Saguinus oedipus) and Old World Monkeys (Cercopitecus aethiops andMacaca fascicularis). Our data show the presence of a single IgG gene inLemur and probably inS.l oedipus, and of multiple genes in the two Cercopithecinae. These findings suggest that a single IgG gene was present in the ancestor of primates: we suppose that this IgG gene was later duplicated several times during primate evolution.     

Jaw movement and tooth use in recent and fossil primates

Masticatory movements and molar wear facets in species of Tupaia, Galago, Saimiri, and Ateles have been examined using cinefluorography and occlusal analysis. The molars have been compared with those of a fossil series: Palenochtha, Pelycodus and Aegyptopithecus. The extant primates are almost identical in their feeding behaviour, the movements and timing of the masticatory cycle. Food is first puncture-crushed where the cycle is elongated, the power stroke attenuated and abrasion facets are produced on the molars. Chewing follows, the movements are more complex, the power stroke has two distinct parts and attrition facets are produced. In the primitive forms (Tupaia, Palenochtha), shearing blades, arranged in series (en echelon) were used to cut the food during the first part (Phase I) of the power stroke as the lower teeth move into centric occlusion. This mechanism has been progressively replaced by a system of blade-ringed compression chambers which cut and compartmentalise the food in Phase I. This is followed by an anteromedially and inferiorly directed movement away from centric occlusion (Phase II) in which the food is ground. In both extant and fossil series there has been a clear trend towards the elongation of Phase II with a corresponding reduction in Phase I. These results suggest that the observed changes in the morphology of the jaw apparatus have probably occurred within the limits set by a pre-existing behavioral pattern.     

Interspecific perspective on mechanical and nonmechanical models of primate circumorbital morphology.

Linear dimensions and angular orientations of the browridge, postorbital bar, and postorbital septum were obtained from a representative series of primates and compared with variables associated with several nonmechanical and biomechanical/mechanical models put forward to explain the form and function of the circumorbital region. Analyses of the results indicate that face size is the primary determinant of variation in primate circumorbital morphology. Anteroposterior browridge thickness is correlated with neural-orbital disjunction among anthropoid primates, but not among prosimians. This difference appears related to differences in the construction of the upper face and anterior cranial fossa between prosimians and anthropoids. Little support is demonstrated for the anterior dental loading model of browridge development. Mediolateral postorbital bar width and (to a lesser degree) browridge height are correlated with neurofacial torsion during mastication and variation in masticatory muscle size. These analyses further suggest that since circumorbital structures (especially the browridges) are located the farthest away from the chewing apparatus, they are least affected by masticatory stresses.     

The evolution of molar occlusion in the Cercopithecidae and early catarrhines

Those Eocene prosimians which are possible catarrhine ancestors have four blade-like crests on each lower molar. Each crest shears in sequence across two upper molar crests. Occluding crests are concavely curved to hold the foods being sheared. Each of two medial lower molar crests bordering the principal crushing surface shear past single upper molar crests at about the same time the lateral lower molar crests contact the second rank of upper molar crests. Grinding and crushing areas are restricted to hypoconid, trigonid, and protocone surfaces. Oligocene catarrhine molars have increased crushing-grinding capacities and maintained but modify their shearing. As the crushing surface of the protocone expands and a crushing hypocone is added, the “second rank” upper molar shearing crests are functionally reduced. At the same time medial crests are increasingly emphasized so that the total shearing capacity remains virtually unchanged. Marginal shearing blades are straight edged; leading edges of occluding blades are set at different angles to the occlusal plane so that blades contact at only one point at any given time. Early Primates have separate crushing basins surrounded by shearing blades. Catarrhines tend to link expanding crushing surfaces anteroposteriorly into a continuous surface between all molars. A cladistic analysis based on both new and previously recognized characters indicates that: 1, Apidium may be more closely related to Aegyptopithecus than to Parapithecus; 2, cercopithecids are derived from a Parapithecus-related stock; 3, Oreopithecus could equally well have come from an Apidium or Aegyptopithecus stock.     

Telomere Biology and Cellular Aging in Nonhuman Primate Cells

To determine how cellular aging is conserved among primates, we analyzed the replicative potential and telomere shortening in skin fibroblasts of anthropoids and prosimians. The average telomere length of the New World primates Ateles geoffroyi (spider monkey) and Saimiri sciureus (squirrel monkey) and the Old World primates Macaca mulatta (rhesus monkey), Pongo pygmaeus (orangutan), and Pan paniscus (pigmy chimpanzee) ranged from 4 to 16 kb. We found that telomere shortening limits the replicative capacity of anthropoid fibroblasts and that the expression of human telomerase produced telomere elongation and the extension of their in vitro life span. In contrast the prosimian Lemur catta (ring-tailed lemur) had both long and short telomeres and telomere shortening did not provide an absolute barrier to immortalization. Following a transient growth arrest a subset of cells showing a reduced number of chromosomes overgrew the cultures without activation of telomerase. Here we show that the presence of continuous TTAGGG repeats at telomeres and rigorous control of replicative aging by telomere shortening appear to be conserved among anthropoid primates but is less effective in prosimian lemurs.     

A possible role of plantations for primate conservation in Madagascar

The utilization of eucalyptus plantations by seven sympatric species of prosimians was studied in the eastern rainforest of Madagascar. The species were Avahi laniger, Cheirogaleus major, Hapalemur griseus, Indri indri, Lemur fulvus, Lepilemur mustelinus, and Microcebus rufus. None of the lemurs was ever found in young eucalyptus plantations with little undergrowth. This was mainly due to the lack of travel opportunities within the shrub layer and between the shrubs and the canopy. Food (mainly berries) is seasonally available in the shrub layer but cannot be exploited because frugivorous lemurs cannot reach it. Old eucalyptus plantations with dense undergrowth are used by all prosimian species. They provide food as well as travel and resting facilities. Mixed tree plantations in the western part of Madagascar were used by groups of Lemur fulvus, Lepilemur mustelinus, and Propithecus verreauxi. According to these results, old eucalyptus plantations and mixed tree species plantations could be used to provide firewood and construction wood for the human population. They also might extend the habitat for lemurs and serve as buffers against human disturbance.     

A unique form of dental bilophodonty and a functional interpretation of peculiarities in the masticatory system of Arsinoitherium (mammalia,Embrithopoda)

The highly autapomorphic upper molar bilophodonty of the Oligocene mammal, Arsinoitherium (Embrithopoda) is an extreme form of dilambdodonty effected by lingual positioning of normally buccally situated cusps with reduction of lingual cusps. This effectively limits the molar dentition to a single phase shearing occlusal motion. Molar and premolar morphology is very different, premolars exhibiting high longitudinal ectolophs and typical two phase occlusal morphology. A double faceted mandibular condyle and angular discontinuity between lower molar and premolar dentitions is interpreted as a means of separating premolar from molar occlusion. A bifunctional masticatory system is proposed whereby efficient premolar occlusion is achieved only after a repositioning of the temporomandibular joint. Loss of phase II occlusion in the molars is compensated by maintenance of a crushing/grinding mode in the premolars. This coupled with the ability to maintain high occlusal pressures along the length of the mandible explains the unbroken dental arcade. Arsinoitheres therefore possess an extremely specialised masticatory apparatus and are interpreted as highly selective browsing herbivores.     

An analysis of chewed food particle size and its relationship to molar structure in the primatesCheirogaleus medius andGalago senegalensis and the insectivoranTupaia glis

The chewed food particle size and shearing capacity of the lower molars of two primate species, the fat-tailed dwarf lemur,Cheirogaleus medius and the bushbabyGalago senegalensis, and an insectivoran, the tree shrew,Tupaia glis, were compared. Differences in the shearing design of the lower molars correlate strongly with the chewed food particle size in these species: the greater the shearing capacity, the smaller the chewed food particles. These three species are of comparable size but differ greatly in diet in the wild.C. medius primarily eats fruit and nectar, whileG. senegalensis andT. glis are largely insect-eaters. The lower molars ofG. senegalensis andT. glis show a much greater shearing capacity than do those ofC. medius. The average length of chewed food particles ofC. medius is significantly larger than that ofG. senegalensis, while that ofT. glis is intermediate between the two primates but is closer to that ofG. senegalensis. Our findings that insect-eating species grind their food more finely than do fruit- and resin-eating species can be correlated with digestibility of foods: finely chewing foods such as fruits which are low in relatively undigestible cell wall components would not greatly improve their digestibility, so a highly efficient food processing apparatus would be less important to the animal's survival. Insect-eaters much more finely chew their foods, implying that there is some constituent of insect bodies difficult to digest, and that grinding increases its digestibility. We suggest that this constituent is chitin.     

Bite force and occlusal stress production in hominin evolution

Maximum bite force affects craniofacial morphology and an organism's ability to break down foods with different material properties. Humans are generally believed to produce low bite forces and spend less time chewing compared with other apes because advances in mechanical and thermal food processing techniques alter food material properties in such a way as to reduce overall masticatory effort. However, when hominins began regularly consuming mechanically processed or cooked diets is not known. Here, we apply a model for estimating maximum bite forces and stresses at the second molar in modern human, nonhuman primate, and hominin skulls that incorporates skeletal data along with species‐specific estimates of jaw muscle architecture. The model, which reliably estimates bite forces, shows a significant relationship between second molar bite force and second molar area across species but does not confirm our hypothesis of isometry. Specimens in the genus Homo fall below the regression line describing the relationship between bite force and molar area for nonhuman anthropoids and australopiths. These results suggest that Homo species generate maximum bite forces below those predicted based on scaling among australopiths and nonhuman primates. Because this decline occurred before evidence for cooking, we hypothesize that selection for lower bite force production was likely made possible by an increased reliance on nonthermal food processing. However, given substantial variability among in vivo bite force magnitudes measured in humans, environmental effects, especially variations in food mechanical properties, may also be a factor. The results also suggest that australopiths had ape‐like bite force capabilities. Am J Phys Anthropol 151:544–557, 2013. © 2013 Wiley Periodicals, Inc.     

Evolution of the primate cytochrome c oxidase subunit II gene

We examined the nucleotide and amino acid sequence variation of the cytochrome c oxidase subunit II (COII) gene from 25 primates (4 hominoids, 8 Old World monkeys, 2 New World monkeys, 2 tarsiers, 7 lemuriforms, 2 lorisiforms). Marginal support was found for three phylogenetic conclusions: (1) sister-group relationship between tarsiers and a monkey/ape clade, (2) placement of the aye-aye (Daubentonia) sister to all other strepsirhine primates, and (3) rejection of a sister-group relationship of dwarf lemurs (i.e., Cheirogaleus) with lorisiform primates. Stronger support was found for a sister-group relationship between the ring-tail lemur (Lemur catta) and the gentle lemurs (Hapalemur). In congruence with previous studies on COII, we found that the monkeys and apes have undergone a nearly two-fold increase in the rate of amino acid replacement relative to other primates. Although functionally important amino acids are generally conserved among all primates, the acceleration in amino acid replacements in higher primates is associated with increased variation in the amino terminal end of the protein. Additionally, the replacement of two carboxyl-bearing residues (glutamate and aspartate) at positions 114 and 115 may provide a partial explanation for the poor enzyme kinetics in cross-reactions between the cytochromes c and cytochrome c oxidases of higher primates and other mammals. Correspondence to: R.L. Honeycutt     

Baculum length and copulatory behavior in primates

The length of the baculum (os penis) was measured in 74 adult males representing 46 primate species. These data, and a review of previously published measurements, indicate that variation in baculum length among primates is related to taxonomic and behavioral differences. Thus, many New World monkeys have shorter bacula, relative to body weight, than Old World monkeys. The baculum is shorter in colobine monkeys than in cercopithecines. Among the great apes, reduction of the baculum is more pronounced in Pan and Gorilla than in Pongo. Very long bacula are found in some nocturnal prosimians (eg, Lorisidae) and also in Macaca arctoides. A comparison of baculum length relative to body weight was made in 34 species for which detailed information on copulatory behavi or was available. The presence of an elongated baculum was shown to correlate with copulatory patterns involving prolonged intromission and/or the maintenance of intromission during the postejaculatory interval (eg, Galago crassicaudatus, Loris tardigradus, M, arctoides). The evolutionary significance of these observations is discussed and it is suggeted that similar copulatory patterns may occur in species with elongated bacula (eg, Daubentonia, Perodicticus) for which behavioral data are lacking at present. The same hypothesis also applies to an extinct adapid primate which possessed a very large baculum.