Inter- and intra-specific gene-density-correlated radial chromosome territory arrangements are conserved in Old World monkeys

Recently it has been shown that the gene-density correlated radial distribution of human 18 and 19 homologous chromosome territories (CTs) is conserved in higher primates in spite of chromosomal rearrangements that occurred during evolution. However, these observations were limited to apes and New World monkey species. In order to provide further evidence for the evolutionary conservation of gene-density-correlated CT arrangements, we extended our previous study to Old World monkeys. They comprise the remaining species group to be analyzed in order to obtain a comprehensive overview of the nuclear topology of human 18 and 19 homologous CTs in higher primates. In the present study we investigated four lymphoblastoid cell lines from three species of Old World monkeys by three-dimensional fluorescence in situ hybridization (3D-FISH): two individuals of Japanese macaque (Macaca fuscata), crab-eating macaque (Macaca fascicularis), and an interspecies hybrid individual between African green monkey (Cercopithecus aethiops) and Patas monkey (Erythrocebus patas). Our data demonstrate that gene-poor human 18 homologous CTs are located preferentially close to the nuclear periphery, whereas gene-dense human 19 homologous CTs are oriented towards the nuclear center in all cell lines analyzed. The gene-density-correlated positioning of human 18 and 19 homologous CTs is evolutionarily conserved throughout all major higher primate lineages, despite chromosomal inversions, fusions, fissions or reciprocal translocations that occurred in the course of evolution in these species. This remarkable preservation of a gene-density-correlated chromatin arrangement gives further support for a functionally relevant higher-order chromatin architecture.     

Diet for a small primate: Insectivory and gummivory in the (large) patas monkey (Erythrocebus patas pyrrhonotus)

A 17 month field study of unprovisioned patas monkeys (Erythrocebus patas pyrrhonotus) in Laikipia, Kenya, using both ad libitum and scan sampling techniques, revealed that the diet of patas monkeys consists primarily of gum of Acacia drepanolobium, arthropods (both free-living and concentrated in the swollen thorns of A. Drepanolobium), and other animals. This type of diet is normally found only in smaller-bodied primates. Results from vegetational transects suggest that the larger-bodied patas monkey can subsist on such a diet because gum and arthropods are relatively easily found in their habitat, thereby minimizing search time. Patas monkeys also spend more time moving and less time feeding (while not moving) than other Old World primates. The characteristic long limbs of patas may have evolved in response to feeding on small, nonusurpable, and widely distributed foods, in which access to foods is maximized while time and energy spent in terrestrial travel between food sites are minimized. Am. J. Primatol. 45:381–398, 1998. © 1998 Wiley-Liss, Inc.     

Developmental trends in mother-infant interactions in Java macaques (Macaca fascicularis) during the first ten days of life

In this study on Java macaques themain characteristics of the mother-infant relationship during infants' first 10 days have been elaborated. Early mother and infant behaviour is described and early interactions between mothers and their young have been analyzed. Observations and trend analyses of early behaviours like ventro-ventral contact behaviour, being on nipple, and explorative behaviour, make it clear that Java macaque infants play an important role in the early development of mother-infant interactions. In contrast to the rhesus and the stumptailed infant, the young Java macaque appears to develop a great variety of behaviours in its first 10 days. Whereas the infant's behaviour gains in complexity and social initiative, the mother becomes increasingly more passive and self-oriented. Early mother-infant interaction can be characterized by mutual adjustment.     

Fibrinopeptides A and B of Japanese monkey (Macaca fuscata) and patas monkey (Erythrocebus patas): their amino acid sequences, restricted mutations, and a molecular phylogeny for macaques, guenons, and baboons

Amino acid sequences of fibrinopeptides A and B from the macaque, Macaca fuscata (Japanese monkey) and the guenon, Erythrocebus patas (patas monkey) were established. Fibrinopeptides A of the monkeys had a sequence identical with those of baboons: Ala-Asp-Thr-Gly-Glu-Gly-Asp-Phe-Leu-Ala-Glu-Gly-Gly-Gly-Val-Arg. Fibrinopeptides B were 9-residue, "short," peptides with the sequences Asn-Glu-Glu-Ser-Leu-Phe-Ser-Gly-Arg for M. fuscata and Asn-Glu-Glu-Val-Leu-Phe-Gly-Gly-Arg for E. patas. The sequence of the B peptide of M. fuscata differed from that of a close-related species, M. mulatta (rhesus monkey), at a single site, Leu (M.f.)----Pro (M.m.). A single replacement between the B peptides of E. patas and Cercocebus aethiops (green monkey), Val (E.p.)----Gly (C.a.), was detected. A phylogenic relationship of macaques, guenons, and baboons, named Cercopithecinae (Old World monkey), was deduced from the sequence data. A selective rather than random amino acid replacement was observed in the B peptides of these Old World monkeys, suggesting a restricted mutation of their fibrinopeptides during primate evolution.     

Allomothering behaviour of new and old world monkeys

The holding or transferring of newborn infants at less than 1 month old by individuals other than the mothers was studied in 24 species of New and Old World monkeys under captive conditions. The observed monkey species could be divided into two types. Group A included eight species of three families where the mothers were tolerant to ‘infant transfer’ and readily retrieved their infants from other individuals, the frequency of infant transfer being high. The infant transfer of this group was termed allomothering behaviour. Group B included 16 species of two families where infant transfer did not occur at all or its frequency was very low and the mothers were possessive of their infants. Once transfer did occur, the infant could not be reclaimed with ease. The relationships between the two groups and taxonomic status, life forms and social types were evaluated in a total of 45 species from the present study and the literature. Correspondences were found with social type and taxonomic status. That is, species of Group A were seen only in the family or one-male type, except for one species, although none of this group appeared in the Cercopithecinae regardless of social types. The significance of infant transfer is discussed in relation to the participants' responses to it and the correlations between the two groups and social types.     

神农架川金丝猴投食群0-6月龄的母亲照顾行为

与其它哺乳动物相比,灵长类动物的一个最典型的特征就是婴儿在出生之后完全没有独立生活能力,处于这个时期的动物非常软弱(Nicolson,1987)。在这段发育期内,必须依靠社群内成年或亚成年个体的照顾才能顺利存活,尤其是来自母亲的照顾,母亲通过哺乳提供给它们成长所需要的营养,并通过限制行为实施保护,同时教会婴儿基本的生存技能,为今后能更好地融入社群做好充足准     

Maternal Behavior and Infant Congenital Limb Malformation in a Free-Ranging Group of <Emphasis Type="Italic">Macaca fuscata</Emphasis> on Awaji Island,Japan

We studied the relationship between maternal behavior and infant disability in 12 mother-infant dyads for the first 5 weeks of infant life in the free-ranging Japanese macaque (Macaca fuscata) group on Awaji Island, Japan, from May to September 2001. Congenital limb malformations are prevalent in this population, and as such carry implications for behavior and conservation. We did not detect any differences in maternal activity budgets, mother-infant physical contact, infant holding, and overall nursing and infant transport time between mothers of non-disabled infants, disabled infants that were able to cling to their mothers, and disabled infants whose limb structure prevented clinging. Mothers of infants with limb malformations severe enough to prevent normal clinging behavior manually supported their infants during nursing and locomotion significantly more than other mothers did theirs. Increased support-carrying and support-nursing, and higher frequencies of holding the infant to one's ventrum, suggest that mothers of extensively malformed infants may be investing more to facilitate the survival of their offspring and that infant disability appears to be influencing maternal behaviors in this population.     

Mother-infant interactions of wild-born,individually-caged cynomolgus monkeys (Macaca fascicularis) during the first 14 weeks of infant life

This study documents age-related changes in the interactions of wild-born cynomolgus macaque mothers and their infants living in individual cages during the first 14 weeks of infant life. Body contact between mother and infant, maternal holding, and infant sucking were found to decrease, and the mothers showed an increased frequency of aggression toward their infants with age. These results were broadly similar to those reported for mother-infant interactions in other macaques living in social groups. Nevertheless, a clear difference between the present cynomolgus macaques and other macaques in social groups was apparent. The cynomolgus macaque mothers tended to permit their infants to move about freely without displaying maternal protectiveness such as restraint or retrieval, unlike other macaque mothers in social groups. Such maternal behaviors might derive from the experience of living in individual cages for many years and the relative safety of living in individual cages. The lack of maternal restraint and retrieval could be responsible for the observed sex differences in behavior: male infants moved more actively, and broke, and made contact with their mothers more frequently than did female infants. Moreover, mothers of female infants held and groomed them more frequently and were less aggressive toward them.     

Phylogeny of African monkeys based upon mitochondrial 12S rRNA sequences

The suborder Anthropoidea of the primates has traditionally been divided in three superfamilies: the Hominoidea (apes and humans) and the Cercopithecoidea (Old World monkeys), together comprising the infraorder Catarrhini, and the Ceboidea (New World monkeys) belonging to the infraorder Platyrrhini.We have sequenced an approximately 390-base-pair part of the mitochondrial 12S rRNA gene for 26 species of the major groups of African monkeys and apes and constructed an extensive phylogeny based upon DNA evidence. Not only is this phylogeny of great importance in classification of African guenons, but it also suggests rearrangements in traditional monkey taxonomy and evolution. Baboons and mandrills were found to be not directly related, while we could confirm that the known four superspecies of mangabeys do not form a monophyletic group, but should be separated into two genera, one clustering with baboons and the other with mandrills. Patas monkeys are clearly related to members of the genus Cercopithecus despite their divergence in build and habitat, while the talapoin falls outside the Cercopithecus clade (including the patas monkey). Correspondence to: A.C. van der Kuyl     

MOTHER-INFANT SPATIAL RELATIONS IN CAPTIVE BOTTLENOSE DOLPHINS,TURSIOPS TRUNCATUS

The prolonged nursing period and strong, extended mother-infant bond observed among bottlenose dolphins may reflect social and physical ontogeny critical for infant survival. This study was conducted to quantify ontogentic changes in mother-infant contact time and the amount of time infants spent in specific spatial states with their mothers from birth to age 12 mo. These behaviors were studied through a systematic, longitudinal study of six mother-infant pairs of captive bottlenose dolphins from three different social groups. There was a significant decrease in the time infants spent with their mothers (logistic regression, P < 0.001), following the general mammalian pattern of increasing independence with age. When with their mothers, the probability that infants would be found in “echelon” position, flanking the mother, decreased as the calf aged (logistic regression, P <0.001), possibly due to anatomical and hydrodynamic factors. The probability that infants would be found in “infant” position, underneath the mother, increased with calf age (logistic regression, P < 0.001). Results obtained in this study are consistent with similar studies of wild bottlenose dolphin mother-infant pairs, indicating a suite of ontogenetically comparable behaviors between wild and captive bottlenose dolphins.     

Playback experiment to test maternal responses of Japanese macaques (Macaca fuscata) to their own infant's call when the infants were four to six months old

Calls emitted by infants when the infant loses sight of its parents are useful to estimate the infant's requirement for parental care. When an Old World monkey infant loses sight of its mother it emits whistles. Therefore, it would be interesting to determine whether mothers could distinguish their own infant's whistles from the whistles of other infants. The response of each of seven Japanese macaque (Macaca fuscata) mothers to her own infant's whistle was compared with their responses to another infant's whistle. Matched control playback experiments were performed when the infants were four to six months old. The results showed that each mother could distinguish her own infant's whistle from that of another infant when the infants were four to six months old. Although a stricter experimental plan is required to further examine the issue, we found that the dominance rank of the infant's mother was another important factor in the female response to the infant's call. The finding suggests that females can associate a call emitted by an infant with its mother's rank, even before the infant begins to wander far from its mother.     

Weaning Age,Infant Care,and Behavioral Development in <Emphasis Type="Italic">Trachypithecus leucocephalus</Emphasis>

Primate infants are born in an altricial state and rely on the care of their parents for a relatively long period of time. Parental investment is critical to offspring survival and thus to the reproductive success of the parent as well. However, mothers and infants may experience a conflict of interest, in that infants may benefit by receiving prolonged maternal care but mothers may curtail such care in a tradeoff between investment in current versus future offspring. Documenting life history characteristics, such as age at weaning, is important not only for understanding the conflicts of interest and tradeoffs; such information can also provide insights about female reproductive rates and be valuable for conservation efforts. Little is known about the life history of white-headed langurs (Trachypithecus leucocephalus), despite their endangered status. We were the first to investigate mother-infant relationships and infant behavioral development in the species. We studied 3 wild mother-infant pairs throughout infancy. We used data from >460 h of focal subject sampling to calculate the proportion of time individuals spent in different behavioral states and the frequency of instantaneous events, such as maternal rejection. White-headed langur infants depended on their mothers for 19–21 mo, at which time they were weaned. Maternal rejection facilitated infant independence in the early stages of infant development, and mothers stopped investing in their infants when they resumed estrus. The weaning age of the wild white-headed langurs we studied was dramatically longer than that of captives, possibly as a result of the nutritional differences between wild and captive populations. Weaning age was also longer than for most other Asian colobines, and may be attributable to the degradation and fragmentation of their natural habitat.     

Social development in three species of macaque (Macaca mulatta, M. fascicularis, M. tonkeana): A preliminary report on the first ten weeks of life

The development of social relations was studied in 11 infant monkeys over the first ten weeks of life : 5 subjects in a rhesus macaque group ($\text{Macaca mulatta}$), 3 in a long-tailed macaque group ($\text{M. fascicularis}$) and 3 in a Tonkean macaque group ($\text{M. tonkeana}$). Tonkean infants were found to interact with many different group members because of the permissiveness of their mothers, while social contacts of rhesus and long-tailed infants are less varied due to the restrictiveness of their mothers. These differences were consistent with patterns of adult-adult interactions, Tonkean macaques showing less intense agonistic interactions than the other two species.     

Nutritional benefits of crematogaster mimosae ants and acacia drepanolobium gum for patas monkeys and vervets in laikipia,Kenya

Patas monkeys (Erythrocebus patas) are midsized primates that feed extensively on the gum of Acacia drepanolobium and the ants are housed in swollen thorns of this Acacia. Their diet resembles that expected more of smaller bodied primates. Patas monkeys are also more like smaller bodied primates in reproducing at high rates. We sought to better understand the convergence of patas monkeys with smaller bodied primates by comparing their feeding behavior on ants and gum with that of closely related, sympatric vervets (Chlorocebus pygerythrus), and analyzing the nutrient content of the gum of A. drepanolobium and of Crematogaster mimosae, the most common ant species eaten by patas monkeys in Laikipia, Kenya. All occurrences of feeding and moving during focal animal sampling revealed that 1) patas monkeys seek A. drepanolobium gum but vervets avoid it; 2) both species open swollen thorns most often in the morning when antsare less active; 3) patas monkeys continually feed onswollen thorns and gum while moving quickly throughout the day, whereas vervets reduce their consumption of these items and their travel rate at mid‐day, and; 4) vervets eat young swollen thorns at a higher rate than patas monkeys. Patas monkeys are able to spend little time acquiring substantial amounts of energy, protein, and minerals from A. drepanolobium gum and C. mimosae ants each day. These findings, when coupled with evidence of causes of infant and adult female mortality, suggest that reproductive success of female patas monkeys is more immediately affected by illness, disease, interactions between adults and infants, and access to water than by food. Am J Phys Anthropol, 2013. © 2012 Wiley Periodicals, Inc.     

Estimates of milk constituents from lactating bonnet macaque (Macaca radiata) mothers between two and seven months post‐partum

Background The literature regarding milk composition in non‐human primates collected across offspring development is limited. We assayed milk samples from bonnet macaque (Macaca radiata) mothers as part of studies characterizing development of this species. Methods Milk was obtained when possible longitudinally from seven lactating bonnet macaque mothers. Samples were frozen until analysis. Individual samples were analyzed to determine the concentrations of electrolytes including sodium, potassium, calcium, chloride, and magnesium, as well as urea, protein, lipids, glucose, and lactose. Results A trend for increased lipids as well as protein percentage was noted with increasing infant age. Chloride and calcium showed an increase with age, whereas other electrolytes remained relatively stable across development. Conclusions The composition of the milk of this particular macaque species was similar to other Old World primates as well as humans. These data add to the limited information available on milk constituents among mammals.     

Artificial weaning of Old World monkeys: benefits and costs

Permanent mother-infant separation prior to natural weaning is a common hus-bandry practice in monkey breeding colonies. In the United States, all eight Re-gional Primate Research Centers have such colonies. Under undisturbed conditions, Old World monkey mothers wean their infants at the age of about 1 year (Hall & DeVore, 1965; Poirier, 1970; Roonwal & Mohnot, 1977; Southwick, Beg, & Siddiqi, 1965). Natural weaning is a gradual process. It implies that the mother, over a period of several weeks or months, more and more consistently discourages her infant to suck on her breasts. Once the mother stops nursing the infant for good, the affectionate bond between the two is not broken (Altmann, Altmann, Hausfater, & McCuskey, 1977; Lindburg, 1971; Poirier, 1970; Roonwal & Mohnot, 1977). The young usually remains in the ma-ternal group at least until prepuberty. Under confinement conditions, artificial weaning is an abrupt occurrence that takes place several months prior to the biologically normal age of weaning. It im-plies that the still-nursed infant is taken away from the mother and subsequently reared alone or with other artificially weaned infants.     

Longitudinal observations of care and development of infant titi monkeys (Callicebus moloch)

The purpose of this study was to describe patterns of infant care and development in family groups of the monogamous titi (Callicebus moloch). Three infant titis were observed with their natal family groups over the first six months of life. Field observations of extensive male involvement with infants were confirmed. Adult males were clearly the infants' primary social companions, and infants spent more time in contact with adult males at all ages than with mothers or older siblings. However, mothers and siblings also carried infants at times and interacted with them in affiliative ways (e.g., grooming, nuzzling, play). Mothers often invited nursing, but otherwise it was infants who primarily initiated transfers between carriers and approaches to parents, reminding us that the infants' own activities and their effects on caregivers should not be overlooked in considerations of the patterns of infant care. This is particularly important for those species exhibiting extensive parental involvement by males. It is suggested that substantial male care of young titi infants leads to several important consequences for the infant's social development, including the development of a stronger attachment to the father than the mother.     

Evolution of an intronic microsatellite polymorphism in Toll-like receptor 2 among primates

Nonhuman primates express varying responses to Mycobacterium tuberculosis: New World monkeys appear to be resistant to tuberculosis (TB) while Old World monkeys seem to be particularly susceptible. The aim of this study was to elucidate the presence of the regulatory guanine–thymine (GT) repeat polymorphisms in intron 2 of Toll-like receptor 2 (TLR2) associated with the development of TB in humans and to determine any variations in these microsatellite polymorphisms in primates. We sequenced the region encompassing the regulatory GT repeat microsatellites in intron 2 of TLR2 in 12 different nonhuman primates using polymerase chain reaction amplification, TA cloning, and automatic sequencing. The nonhuman primates included for this study were as follows: chimpanzee (Pan troglodytes), bonobo (Pan paniscus), gorilla (Gorilla gorilla), orangutan (Pongo pygmaeus), Celebes ape (Macaca nigra), rhesus monkey (Macaca mulatta), pigtail macaque (Macaca nemestrina), patas monkey (Erythrocebus patas), spider monkey (Ateles geoffroyi), Woolly monkey (Lagothrix lagotricha), tamarin (Saguinus labiatus), and ring-tailed lemur (Lemur catta). Nucleotide sequences encompassing the regulatory GT repeat region are similar across species and are completely conserved in great apes. However, Old World monkeys lack GT repeats altogether, while New World monkeys and ring-tailed lemurs have much more complex structures around the position of the repeats. In conclusion, the genetic structures encompassing the regulatory GT repeats in intron 2 of human TLR2 are similar among nonhuman primates. The sequence is most conserved in New World monkeys and less in Old World monkeys.     

Demography and Life Histories of Sympatric Patas Monkeys, <Emphasis Type="Italic">Erythrocebus patas</Emphasis>, and Vervets, <Emphasis Type="Italic">Cercopithecus aethiops</Emphasis>, in Laikipia,Kenya

Mortality patterns are thought to be strong selective forces on life history traits, with high adult mortality and low immature mortality favoring early and rapid reproduction. Patas monkeys (Erythrocebus patas) have the highest potential rates of population increase for their body size of any haplorhine primate because they reproduce both earlier and more often. We report here 10 yr of comparative demographic data on a population of patas monkeys and a sympatric population of vervet monkeys (Cercopithecus aethiops), a closely related species differing in aspects of social system, ecology, and life history. The data reveal that 1) adult female patas monkeys have significantly higher mortality than adult female vervets; 2) infant mortality in patas monkeys is relatively low compared to the norm for mammals because it is not significantly different from that of adult female patas monkeys; and 3) infant mortality is significantly higher than adult female mortality in vervets. For both species, much of the mortality could be attributed to predation. An epidemic illness was also a major contributor to the mortality of adult female patas monkeys whereas chronic exposure to pathogens in a cold and damp microenvironment may have contributed to the mortality of infant vervets. Both populations experienced large fluctuations during the study period. Our results support the prediction from demographic models of life history evolution that high adult mortality relative to immature mortality selects for early maturation.     

Maternal Anxiety in Rhesus Macaques (Macaca mulatta)

Visual monitoring and scratching were used as behavioral indicators of maternal and social anxiety in small captive groups of rhesus macaques. Young infants were especially at risk from other group members during the first weeks of locomotion away from their mothers. Mothers received aggression from other individuals irrespective of their infants' presence or absence. The rate at which mothers scratched themselves increased significantly when their infants moved away from them and when the infants approached or were approached by individuals who frequently harassed them. The rate of maternal scratching and the rate of glancing at the infant and at other individuals when the infant was away decreased as infants grew older and became less vulnerable to harassment. In contrast, the rate of maternal scratching and visual monitoring of other individuals when the infant was in contact remained stable across the first 12 wk of lactation. The rate of maternal scratching increased when the mother-infant pair was in spatial proximity to the adult male or higher ranking adult females. Although visual monitoring and scratching showed a similar sensitivity to social variables, it is speculated that they might reflect different components of anxiety, namely, anticipation of danger and uncertainty due to motivational conflict. The results of this investigation indicate that a macaque mother's emotional reactivity to a perceived danger for herself and her infant can be measured quite accurately using the rates of visual monitoring and scratching and that the latter represent reliable tools to investigate the emotional correlates of maternal behavior in nonhuman primates.