Patterns of paternal care in primates

An interspecific comparison was carried out to understand better the relationships among paternal care, paternal certainty, and reproductive burden in primates. Although monogamy is generally rare among mammals, a number of primate species are monogamous. Extensive paternal care is a related issue but is one that is not necessarily associated with monogamy or with paternal certainty. For example, despite paternal certainty, primate mothers in monogamous species with body weights over 2 kg still remain the primary infant caretakers, while males in the communally breeding tamarins carry infants more frequently than mothers do, even in the absence of paternal certainty. Several different tactics are used by small-bodied primates to cope with the energetic burden of raising proportionately large infants in an arboreal environment: (1) infant carrying by subadult and/or related nulliparous females (Saimiri, Lemur monogoz); (2) infant carrying by fathers and offspring (Aotus, Callicebus, Saguinus, Cebuella, Leontopithecus); (3) parking infants while family members forage (Tarsius, Galago, Microcebus, Cheirogaleus, Varecia); or (4) some combination of the above (Callithrix, Hapalemur, Loris). Lactation length and infant growth patterns appear to influence which of these tactics is employed by a given species. Moreover, although most small-bodied, mated, monogamous female primates spend no more than 9 months annually in gestation and lactation,Aotus andCallicebus mated females are either pregnant or lactating on a year-round basis. It is this heavy female reproductive burden that may be an important factor in selection for extensive paternal care in these monogamous cebids.     

Ontogeny and homology of the paranasal sinuses in Platyrrhini (Mammalia: Primates)

The identity and taxonomic distribution of paranasal sinuses among living platyrrhines has remained a contentious issue (e.g., Cave [1967] Am J Phys Anthropol 26:277-288 vs. Hershkovitz [1977] Chicago: University of Chicago Press) largely because the ontogenetic data required for their detection and identification (e.g., Cave [1967]; Maier [2000] Cambridge, UK: Cambridge University Press, 99-132.) were not attainable without sacrificing valuable juvenile and subadult specimens. Non-invasive computed tomography (CT) scanning of ontogenetic series of skulls for 10 platyrrhine genera demonstrates the presence of maxillary and ethmoid sinuses, as well as homologs of the human sphenoid and frontal sinuses. Differences in the latter two sinuses between platyrrhines and hominoids highlight the need for early developmental data in establishing sinus homology. In particular, the identification of homologous recesses in the cartilaginous nasal capsule, from which sinuses later develop, emerges as the critical step. This developmental approach also reveals that the anterior and posterior ethmoid sinuses are each sets of serial homologs, a point which reconciles previous difficulties in establishing sinus homologies across mammalian orders (e.g., Paulli [1900] Gegenbaurs Morphol Jahrb 28:147-178, 179-251, 483-564).     

Platyrrhine incisors and diet

Despite the relatively large size of anthropoid incisors in relation to the remainder of the dental arcade, and their prominent role in the preprocessing of food prior to ingestion, comparatively little is known about the functional morphology of anthropoid incisor shape and crown curvature. The relationship between incisor allometry and diet is well documented for both platyrrhines and catarrhines; however, similar relationships between incisor shape and crown curvature have to date only been reported for living and fossil members of the superfamily Hominoidea. Given the limited taxonomic diversity among the extant members of that group, it is difficult to firmly establish the relative influence of phylogeny and dietary function in the governance of incisor crown curvature. Unlike hominoids, which are represented by only five living genera, extant platyrrhines are a more varied group that includes 16 ecologically diverse genera. In an effort to clarify the functional relationship between maxillary and mandibular incisor crown curvature and diet, this study uses high resolution polynomial curve fitting to quantify mesiodistal and cervicoincisal curvature for a taxonomically diverse platyrrhine sample (n = 133 individuals representing 18 taxa) with well documented dietary behavior. Results were consistent with prior analyses of hominoid incisor curvature and identify a significant and positive correlation between incisor crown curvature and diet such that increasing curvature is associated with a proportionate increase in frugivory. These results are independent confirmation of the results reported from a previous analysis of hominoid incisor curvature and provide new evidence to suggest that diet is the primary governing factor influencing anthropoid incisor curvature.     

Characterization of opsin gene alleles affecting color vision in a wild population of titi monkeys (Callicebus brunneus)

The color vision of most platyrrhine primates is determined by alleles at the polymorphic X-linked locus coding for the opsin responsible for the middle- to long-wavelength (M/L) cone photopigment. Females who are heterozygous at the locus have trichromatic vision, whereas homozygous females and all males are dichromatic. This study characterized the opsin alleles in a wild population of the socially monogamous platyrrhine monkey Callicebus brunneus (the brown titi monkey), a primate that an earlier study suggests may possess an unusual number of alleles at this locus and thus may be a subject of special interest in the study of primate color vision. Direct sequencing of regions of the M/L opsin gene using feces-, blood-, and saliva-derived DNA obtained from 14 individuals yielded evidence for the presence of three functionally distinct alleles, corresponding to the most common M/L photopigment variants inferred from a physiological study of cone spectral sensitivity in captive Callicebus.     

Long-term Study of Group Dynamics and Female Reproduction in Venezuelan Pithecia pithecia

White-faced sakis (Pithecia pithecia) are well known for their specialized feeding strategy and dependence on seed-eating, but we know less about social dynamics and reproduction. I summarize data from 1990 to 2001 on sakis inhabiting a small island in Lago Guri, Venezuela that includes changes in group composition, aggressive behavior, and female reproductive histories. Though the characteristic group size and typical mating system are still uncertain for wild, free-ranging Pithecia spp., size of the study group ranged from 2–3 adult females and 1–4 adult males. My group and I collected fecal samples from adult females, which we dried and assayed for estrogen (E₁C) and progesterone (PdG) conjugates to document reproductive cycles and female development. During the study, as many as 3 females were either cycling or pregnant at the same time. Ten infants were born during the study, 4 of which survived to adulthood. Five interbirth intervals after weaning an infant ranged from 12 to 36 mo. Though researchers often assume Pithecia spp. are monogamous, multiple breeding females can coexist in groups without evidence of reproductive suppression. Within the pitheciine clade, Pithecia spp. exhibit a mosaic of behavioral and morphological traits intermediate between bearded sakis and uakaris on the one hand and their sister-group, the pair-bonded titis, on the other.     

Diet of the northern bearded saki (Chiropotes satanas chiropotes): A neotropical seed predator

Data on the diet of Chiropotes satanas chiropotes, the northern bearded saki, has been collected during several years of primate field observations in the Raleighvallen-Voltzberg Reserve in Suriname. This species feeds predominantly on immature seeds and ripe fruit, mainly the former. Chiropotes is especially fond of the members of the Brazil nut family, Lecythidaceae, and other species with exceptionally hard or tough seed pods. Concomitantly, Chiropotes shows striking dental and gnathic adaptations that facilitate opening and ingesting these well-protected food items. Seed predation in the Old World colobine, Colobus satanas, has been discussed primarily as a strategy for survival in forests characterized by leaves with low nutrient content and high toxicity; however, it now appears that arboreal seed predation is a relatively widespread primate dietary strategy found among higher primate species in a variety of forest types on three continents. It is yet another way of “making a living” in a tropical rain forest.     

Development and annotation of shotgun sequence libraries from New World monkeys

The draft genome sequences of several primates are available, providing insights into evolutionary and anthropological research. However, genomic resources from New World monkeys are conspicuously lacking. To date, the genomes of only two platyrrhine species, the common marmoset and the Bolivian squirrel monkey, have been fully sequenced. This is especially limiting for comparative genomics research, considering that New World monkeys are the most speciose primate group, and platyrrhine genetic diversity is comparable to that of the catarrhines (i.e. apes and Old World monkeys). Here, we present the generation and annotation of numerous sequence reads from the genomes of Spider monkey (Ateles belzebuth), Owl monkey (Aotus lemurinus) and Uakari (Cacajao calvus), representing the three platyrrhine families, Atelidae, Cebidae and Pitheciidae, respectively. These sequencing reads were developed from gDNA shotgun libraries containing over 3000 individual sequences with an average length of 726 bps. Of these sequences, 1220 contain <20% repeats, and thus are potentially highly useful phylogenetic markers for other platyrrhine species. Among them, a large number of sequencing reads were found to match unique regions within the human (2462 sequences) and the marmoset (2829 sequences) genomes. In particular, the majority of these sequencing reads are from putatively neutrally evolving intergenic regions. Thus, they are likely to be highly informative for inferring neutral evolutionary patterns and genomic evolution for other New World monkeys.     

Cranial growth in Saimiri sciureus (Cebidae) and its alteration by nutritional factors: A longitudinal study

Ten male Saimiri sciureus boliviensis (Cebidae), born at the Centro Argentino de Primates (CAPRIM), were grown in captivity. At weaning (6 months old), five individuals were fed ad libitum on a 20% protein diet (controls). The other five animals were fed ad libitum on a 5% protein diet (malnourished). Animals were radiographed monthly. The length, width, and height of the anterior, middle, and posterior components of the neurocranium, and those of the masticatory, respiratory, and optic components of the face were measured. A pattern of high growth rate was observed in both the three facial and the middle neural components. The anterior and posterior neural components showed a pattern of low rate of growth. The growth behavior of each variable was also different. Lengths grew more than widths and heights in the facial components, whereas widths grew more than heights and lengths in the neurocranium. Malnutrition delayed growth in size and altered the normal shape changes. High-patterned variables, such as masticatory and respiratory lengths, and the anterior and middle neural widths were particularly affected. The masticatory and the middle neural components underwent the greatest growth arrest. The optic and the respiratory components suffered a mild effect. The anterior and the posterior neural components were affected to a lesser degree. Am J Phys Anthropol 102:545–554, 1997. © 1997 Wiley-Liss, Inc.