Platyrrhine systematics: A simultaneous analysis of molecular and morphological data

Platyrrhine phylogeny has been investigated repeatedly with morphological characters and DNA nuclear gene sequences, with partially inconsistent results. Given the finding in the past decade that the mitochondrial genome is a potentially valuable source of phylogenetic information, we gathered DNA sequence data of a fragment of the 16S and the entire 12S mitochondrial genes. The objectives were to generate a cladistic phylogeny based on these data and to combine them in a simultaneous analysis with morphological characters and preexisting nuclear DNA sequences. Mitochondrial data analyzed on its own yielded a cladogram that was different from those generated with other data sets. The simultaneous analysis of mitochondrial, nuclear, and morphological data yielded a tree most congruent with that generated with nuclear data and to a lesser degree with the morphological one. It depicted a basal dichotomy that led to two major clades: one of them comprised [Atelinae (Callicebus + Pitheciini)] and the other major clade comprised [Aotus ((Cebus, Saimiri) (Callitrichinae))]. The weakest point of the phylogeny was the position of Aotus as basal within their clade as opposed to more closely linked with either the callitrichines or Cebus-Saimiri. Relationships within callitrichines and atelines were unstable as well. The simultaneous phylogenetic analysis of all data sets revealed congruent signal in all of them that was partially obscured in the separate analyses. Am J Phys Anthropol 106:261–281, 1998. © 1998 Wiley-Liss, Inc.     

Response to novelty inSaimiri andCallicebus: Influence of social context

Responses to novel objects by pair-livingSaimiri andCallicebus and grouplivingSaimiri were investigated in two experiments. In the first, titis and squirrel monkeys were tested in the presence and absence of an opposite-sexed pairmate. The species were differentially affected by the absence of the pairmate: titis of both sexes were distressed and object interest was attenuated; squirrel monkeys were not distressed and object scores (particularly females') increased. Nonsocial differences in object exploration principally involved the tempo and mode of investigation; squirrel monkeys were quicker and more vigorous than titis. In the second experiment, presence of a novel object was found to attract and arouse grouplivingSaimiri, as indicated by the change in the frequency and nature of social interactions and spatial distribution. Within- and between-sex social interactions reflected the typical female nucleus-peripheral male pattern seen inSaimiri groups in other environments. Species differences in investigatory patterns were considered to be contributing elements in the maintenance of distinctive life-styles.     

Glucocorticoid enhancement of glucocorticoid production by cultured ovine adrenocortical cells

The present study examines the effect of chronic treatment with glucocorticoids on the steroidogenic activity of ovine adrenocortical cells in vitro. Cells cultured in the presence of 10(-9) to 10(-5) M dexamethasone produced more glucocorticosteroids in response to ACTH1-24, forskolin or 8 BrcAMP than did control cells. Such an enhancing effect required more than 5 h of treatment and was maximal at 30 h; it was both concentration-dependent and steroid-specific. The maximal secretion of corticosteroids was observed when cells were exposed to 10(-7) M dexamethasone; with higher concentrations the response to ACTH1-24 decreased steadily; the ED50 was 2.8 +/- 0.8 nM. Cortisol and corticosterone enhanced ACTH1-24-induced steroidogenesis to the same extent as dexamethasone, but at concentrations roughly 100-fold higher than for dexamethasone. Testosterone and 17 beta-oestradiol had no enhancing effect. Dexamethasone not only enhanced the maximal steroidogenic response to ACTH1-24 but also decreased its ED50 3-fold. Treatment of cultures with the antiglucocorticoid RU 38486 resulted in a dose-dependent, time-dependent, decrease in ACTH1-24-induced corticosteroid output. Moreover, RU 38486 antagonized the enhancing effect of dexamethasone. The production of corticosteroids by dexamethasone-treated cells incubated in the presence of 22(R)-hydroxycholesterol or of exogenous pregnenolone was similar to that of control cells. The enhancing effect of dexamethasone was also observed when cultures were performed in the absence of insulin and/or in serum-free media. These data suggest that chronic exposure to glucocorticoids is necessary for the full steroidogenic activity of ovine adrenocortical cells. Moreover, they indicate that glucocorticoids exert their effect at least at two different levels in the cell: (i) on the adenylate cyclase system and (ii) at step(s) beyond cAMP but before pregnenolone formation.     

Different Rates of LINE-1 (L1) Retrotransposon Amplification and Evolution in New World Monkeys

LINE-1 (L1) elements constitute the major family of retrotransposons in mammalian genomes. Here we report the first investigation of L1 evolution in New World monkeys (NWM). Two regions of the second open-reading frame were analyzed by two methods in three NWM species, the squirrel monkey (Saimiri sciureus), the tamarin (Saguinus oedipus), and the spider monkey (Ateles paniscus). Since these three species diverged, L1 has amplified in the Saimiri and Saguinus lineages but L1 activity seems to have been strongly reduced in the Ateles lineage. In addition, the active L1 lineage has evolved rapidly in Saimiri and Saguinus, generating species-specific subfamilies. In contrast, we found no evidence for a species-specific subfamily in Ateles, a result consistent with the low L1 activity in this species for the last ~25 My.     

A study of postnatal appendicular skeletal maturation in captive-born squirrel monkeys (Saimiri boliviensis)

This study is based on a mixed longitudinal radiographic sampling of appendicular bones in 82 captive-born squirrel monkeys (Saimiri boliviensis). All appendicular ossification centers had appeared radiographically by 17 weeks of age, and epiphyseal fusion was complete by 47-53 months of age. No statistically significant differences were found between the sexes in comparisons carried out at birth and at 6 and 8 months of age. Valid sex comparisons could not be made at other ages owing to the small size of the sample. The sequence of appearance of the ossification centers (Spearman correlation coefficient of Saimiri vs. Callithrix = 0.68) shows greater interspecies differences than the sequence of fusion (Saimiri vs. Callithrix = 0.88).     

Differentiall behavioral and adrenocortical responses to stress among three macaque species

Behavioral and adrenocortical responses of rhesus (Macaca mulatta), bonnet (M. radiata), and crabeating (M. fascicularis) macaques were compared in their home cages, during exposure to novelty and during physical restraint. Both behavioral and adrenocortical responses differentiated species in each condition. In all conditions, post-test corticosteroid levels were highest for crabeaters and lowest for rhesus. Rhesus were the most active behaviorally, and bonnets were the most passive, while crabeaters exhibited the greatest signs of behavioral disturbance. Relationships between adrenocortical and behavioral responses varied between groups. Both adrenocortical and behavioral profiles were in accord with the behavior of these three species under more natural conditions. The role of psychophysiological responses in general behavioral dispositions toward the environment is discussed. It is concluded that behavioral dispositions, inclusive of psychophysiological responses, may vary qualitatively even among closely related primate species.     

Comparison of gut proportions in four small-bodied Amazonian cebids

Gut proportions in four small-bodied Amazonian cebids (Callicebus caligatus, Callicebus moloch, Pithecia irrorata, and Saimiri madeirae) are reported and compared in the context of known differences in feeding ecology. The gastrointestinal tracts of both Callicebus and Pithecia were found to be relatively undifferentiated, as expected from their predominantly frugivorous diets. In Saimiri, the marked dominance of the small intestine correlates with a highly insectivorous diet. © 1995 Wiley-Liss, Inc.     

Adrenocortical responsiveness in southern elephant seal mothers and pups during lactation and the effect of scientific handling

We examined the cortisol responses to chemical and physical restraint stress in southern elephant seal Mirounga leonina females and their pups at three stages during lactation. In anaesthetised females the serum cortisol levels changed moderately during the 45-min sampling period following restraint, with average peaks at 23 min after anaesthetic administration. Overall, cortisol was relatively low 2 days postpartum and increased throughout lactation. In physically restrained pups serum cortisol increased rapidly after capture; the response was milder at age 2 days than at 11 days and 21 days. Levels were higher in female pups than in males. In order to test whether cortisol levels and/or responses became chronically (i.e. days to weeks) altered due to restraint, we compared the cortisol response at a late stage of lactation between three groups of mother-pup pairs previously given different levels of chemical (mothers) or physical (pups) restraint stress: control (not handled previously), moderate treatment (previously handled twice), and high treatment (previously handled 3-4 times). Pups of the three treatment groups showed similar adrenocortical responses suggesting no chronic effect of repeated physical restraint, despite the clear acute effects. Mothers of the control and moderate treatment groups showed similar cortisol responses; however, mothers of the high treatment group showed significantly attenuated responses. This indicated that elephant seals tolerated moderate degrees of handling disturbance; however, repeated (3-4) chemical immobilisations in lactating females may reduce their adrenocortical responsiveness for a period of days or weeks.     

Chronic melatonin treatment and the hypothalamo-pituitary-adrenal axis in the rat: Attenuation of the secretory response to stress and effects on hypothalamic neuropeptide content and release

The pituitary-adrenal secretory response to acute and chronic stress, suppressibility of adrenocortical secretions by exogenous glucocorticoids, and hypothalamic content and in vitro release of the two major peptidergic activators of the hypothalamo-pituitary-adrenal (HPA) axis, corticotropinreleasing hormone (CRH) and arginine-vasopressin (AVP), were examined in rats receiving daily melatonin (MEL) injections coincident with the circadian increment of endogenous pineal and adrenocortical secretory activity. After 7 days of MEL administration, the rats displayed a significant attenuation of the adrenocortical secretory response to acute and chronic stress. Chronic MEL treatment also prevented the decline in adrenocorticotropic hormone (ACTH) release resulting from chronic stress exposure. Hypothalamic CRH content was significantly lower in rats receiving MEL treatment, while AVP remained largely unaltered; however, MEL administration counteracted the chronic stress-induced decrease in hypothalamic AVP content and in vitro release. When exposed to dexamethasone in vitro, hypothalamic explants from MEL-treated rats responded with a stronger suppression of CRH and AVP release than those originating from vehicle-injected animals. These observations indicate that MEL attenuates the adrenocortical response to stress and influences the biosynthesis, release and glucocorticoid responsiveness of hypothalamic ACTH secretagogues.     

Phylogenetic relationships in the genus Cheracebus (Callicebinae,Pitheciidae)

Cheracebus is a new genus of New World primate of the family Pitheciidae, subfamily Callicebinae. Until recently, Cheracebus was classified as the torquatus species group of the genus Callicebus. The genus Cheracebus has six species: C. lucifer, C. lugens, C. regulus, C. medemi, C. torquatus, and C. purinus, which are all endemic to the Amazon biome. Before the present study, there had been no conclusive interpretation of the phylogenetic relationships among most of the Cheracebus species. The present study tests the monophyly of the genus and investigates the relationships among the different Cheracebus species, based on DNA sequencing of 16 mitochondrial and nuclear markers. The phylogenetic analyses were based on Maximum Likelihood, Bayesian Inference, and multispecies coalescent approaches. The divergence times and genetic distances between the Cheracebus taxa were also estimated. The analyses confirmed the monophyly of the genus and a well-supported topology, with the following arrangement: ((C. torquatus, C. lugens), (C. lucifer (C. purinus, C. regulus))). A well-differentiated clade was also identified within part of the geographic range of C. lugens, which warrants further investigation to confirm its taxonomic status.     

Sequences from the 5′ flanking region of the ϵ‐globin gene support the relationship of Callicebus with the pitheciins

The purpose of this study was to determine nucleotide sequences from the 5′ flanking region of the ϵ‐globin gene of selected platyrrhine primates and to analyze the data for phylogenetic information and estimated times of divergence. We report new sequence data for two species of New World monkeys, Callicebus torquatus and Pithecia irrorata. We analyzed these data in conjunction with homologous sequences from other primate species. The data support the hypothesis that the titi monkeys (Callicebus) and seed predators (Tribe Pitheciini) form a clade (Subfamily Pitheciinae), and also provide limited support for that subfamily being allied with the atelines. We also present estimated dates of divergence for the Callicebus and pitheciin lineages. Am. J. Primatol. 48:69–75, 1999. © 1999 Wiley‐Liss, Inc.     

Functional morphology of the postcranium and locomotor behavior of Neosaimiri fieldsi,a Saimiri-like Middle Miocene platyrrhine

A number of postcranial specimens of Neosaimiri fieldsi, a Middle Miocene platyrrhine, were discovered in 1988, 1989, and 1990 at La Venta, Colombia. Until recently only three postcranial specimens of this species had been discovered and the present material adds further information about this taxon's postcranial morphology. In overall skeletal dimensions and in postcranial features, Neosaimiri is most similar to Saimiri among extant medium-sized platyrrhines, but differs from Saimiri in having more rugose surface markings, a longer olecranon, a smaller anterior process of the distal tibia, an absence of a distal surface extension on the anterior tibial shaft, an absence of an anterior midtrochlear depression of the talus, and a shorter distal calcaneus relative to the calcaneal tuberosity. These differences suggest that Neosaimiri was relatively heavily built, possessed a more dominant forelimb in quadrupedal progression, and utilized a less stabilized upper ankle joint, and a shorter power arm for plantarflexion. Neosaimiri is interpreted as an arboreal quadruped with frequent leaping across arboreal gaps, as in extant Saimiri, with perhaps less frequent running and leaping than in Saimiri. As with the dentition, the postcranial specimens suggest the close relationship between Neosaimiri and extant Saimiri. Am J Phys Anthropol 102:515–544, 1997. © 1997 Wiley-Liss, Inc.     

Effect of life history on the squirrel monkey (Platyrrhini,Saimiri) cranium

Among primates, squirrel monkeys uniquely possess an interorbital fenestra, in which the midline bony orbitosphenoid septum is largely absent and the soft tissues of the orbits are separated only by a thin membrane. Neural development may contribute to the approximation of the orbits to the midline in Saimiri, insofar as other platyrrhines with relatively large brains also have relatively narrow interorbital spaces compared to their near relatives. In Saimiri the narrow spacing of the orbits is further exacerbated by intense predation pressure on infants that may select for precocial neonates. The result is a large-headed neonate that is subject to unusual parturition constraints. These parturition constraints apply to the size and dolichocephalic shape of the squirrel monkey head in general, and to the relatively large eyes and approximated orbits in particular. The unique interorbital condition in Saimiri is an example of the effects of life history on skeletal morphology. © 1995 Wiley-Liss, Inc.     

Recovery of Adrenocortical Function during Long-term Treatment with Corticosteroids

The recovery of adrenocortical function during long-term corticosteroid treatment in a group of patients with asthmatic bronchitis was compared with that in a group of patients with sarcoidosis. At corresponding dosages of prednisone basal adrenocortical function as well as adrenocortical response to tetracosactrin stimulation was higher in the asthma patients than in those with sarcoidosis.The rate of recovery of adrenocortical function seems mainly to be determined by the dosage of corticosteroids during the initial stages of treatment rather than by the nature of the disease.     

Characterization of pituitary–adrenocortical activity in the Malayan flying fox (Pteropus vampyrus)

Pituitary–adrenocortical and gonadal endocrine activity was investigated in a captive colony of Pteropus vampyrus, a highly social Old World fruit bat. Both cortisol and corticosterone were present in plasma, at a ratio of approximately 5:1, respectively. Glucocorticoid but not testosterone levels significantly increased prior to and concomitant with the evening active period. Restraint stress for 15–60 min resulted in a significant and rapid increase in plasma levels of adrenocorticotropic hormone (ACTH) and glucocorticoids. ACTH levels quickly returned to baseline following restraint whereas glucocorticoid levels remained elevated for at least 30 min after restraint ended. Plasma ACTH levels after stress were similar to levels reported after stress in other mammals. Stress-induced glucocorticoid levels were several-fold greater than those reported for most mammals. Restraint for 15 min significantly inhibited testosterone levels. Restraint stress did not affect hormone levels on the morning following restraint. Brief capture, handling, and release of the animals did not elicit increases in these hormones. The physiological responsiveness of the pituitary and adrenal glands, along with P. vampyrus’s documented seasonality and range of social behaviors, makes these bats an excellent model for exploring the general physiology of the hypothalamic–pituitary–adrenal and hypothalamic–pituitary–gonadal axes, as well as social influences on these axes.     

Feedback effects of dexamethasone on adrenocortical responses in rats with fornix section.

To investigate the sites of the negative feedback of corticoids in the regulation of ACTH secretion, the effect of 10 mug of dexamethasone on adrenocortical responses to ether stress was studied in intact and fornix-sectioned rats. Dexamethasone pretreatment in both groups depressed significantly both the basal and stress plasma corticosterone levels. However, in rats with fornix section the amount of depression of the adrenocortical response was much smaller than in intact animals, when compared to the non-treated group. These data would inicate that extrahypothalamic regions play a role in the action of glucocorticoids in the feedback control of pituitary-adrenal function and that the hippocampus participates in this mechaism.     

Testing the weekend effect hypothesis: Time of day and lunar phase better predict the timing of births in laboratory‐housed primates than day of week

The weekend effect hypothesis proposes that captive primates are more likely to give birth during times of low disturbance and reduced staff activity. The hypothesis specifically predicts that laboratory‐housed primates will be more likely to give birth during the weekend than weekdays when staff activity is reduced. To date, support for the weekend effect hypothesis has been mixed and based on studies with relatively few subjects. To further examine the hypothesis, we analyzed the birthing patterns of three genera of laboratory‐housed primates: squirrel monkeys (Saimiri species, N = 2,090 births), owl monkeys (Aotus species, N = 479 births), and rhesus macaques (Macaca mulatta, N = 2,047 births). Contrary to predictions derived from the weekend effect hypothesis, the frequencies of births during weekends for all taxa were not significantly different from rates that would be expected by chance. However, while there was no variance across days of the week, all three taxa gave birth at nighttime, when staff was absent. This parallels reports of births in wild and captive monkeys, both diurnal and nocturnal, which are more likely to give birth during the night; plausibly a time when the environmental and social disturbance is lowest and the mother is safest to bond with her newborn infant. As all births occurred at night, we also explored the relationship between the lunar cycle and the timing of births timing. While the diurnal primates (i.e., Saimiri and Macaca) were no more likely to give birth on “bright” nights than “dark” nights, owl monkeys (Aotus) had a much higher frequency of births on bright nights than darker ones, and at rates that deviated from chance. Our data provide a more detailed understanding on how the environment may influence captive monkey births but do not support the oft‐cited weekend effect hypothesis.     

Effects of social isolation and crowding upon adrenocortical reactivity and behavior in the rat

The effects of social isolation and crowding on adrenocortical function and upon behavioral responsiveness to electric shock have been studied in male and female rats. All female experimental groups showed higher corticosterone levels and heavier adrenals than their male counterparts. The major effect of housing condition concerned the corticosterone response to stress, while basal hormone concentration was not modified. Socially housed rats showed a more intense adrenocortical response and also a greater behavioral reactivity to electric shock than the isolates.     

NPY‐Y1 coexpressed with NPY‐Y5 receptors modulate anxiety but not mild social stress response in mice

The Y1 and Y5 receptors for neuropeptide Y have overlapping functions in regulating anxiety. We previously demonstrated that conditional removal of the Y1 receptor in the Y5 receptor expressing neurons in juvenile Npy1r^Y5R?/? mice leads to higher anxiety but no changes in hypothalamus‐pituitary‐adrenocortical axis activity, under basal conditions or after acute restraint stress. In the present study, we used the same conditional system to analyze the specific contribution of limbic neurons coexpressing Y1 and Y5 receptors on the emotional and neuroendocrine responses to social chronic stress, using different housing conditions (isolation vs. group‐housing) as a model. We demonstrated that control Npy1r^2lox male mice housed in groups show increased anxiety and hypothalamus‐pituitary‐adrenocortical axis activity compared with Npy1r^2lox mice isolated for six weeks immediately after weaning. Conversely, Npy1r^Y5R?/? conditional mutants display an anxious‐like behavior but no changes in hypothalamus‐pituitary‐adrenocortical axis activity as compared with their control littermates, independently of housing conditions. These results suggest that group housing constitutes a mild social stress for our B6129S mouse strain and they confirm that the conditional inactivation of Y1 receptors specifically in Y5 receptor containing neurons increases stress‐related anxiety without affecting endocrine stress responses.     

Cranial suture closure in two species of South American monkeys

Cranial suture closure is examined in two species of South American monkeys, Saimiri sciureus and Saguinus nigricollis. Sequences in closure were sought as indicators of skeletal age. Some sutures seem to be more reliable determinants of skeletal age than others, and these sutures and their sequence of closure are different in the two species examined. The sphenooccipital synchondrosis and the palatal portion of the Interpremaxillary suture show regular fusion associated with age in both species. In Saimiri the maxillopremaxillary sutures are also reliable indicators of age, whereas they are not in Saguinus; however, in the latter the presphenoid-postsphenoid synchondrosis closes regularly whereas it does not in Saimiri. In Saimiri the predictable sequence is (1) maxillo-premaxillary, (2) transverse maxillo-premaxillary, (3) spheno-occipital, (4) interpremaxillary. In Saguinus it is (1) presphenoid-postsphenoid, (2) spheno-occipital, (3) interpremaxillary. It is possible that the sequences of suture closure and the variability in this process may indicate genetic and taxonomic relationships.