Cayo Santiago Macaques Research Articles

The Role of Social Group and Matriline on Fluctuating Asymmetry in Female Rhesus Macaques

Fluctuating asymmetry (FA), or random deviations from symmetry, is typically thought to reflect stress during development. Therefore, FA has been used as a proxy for developmental instability in a wide variety of bilaterally symmetric organisms. The literature on FA explores a variety of environmental stressors that invoke mechanisms allowing developmental instability (temperature, food, etc.), but the role of heredity on developmental instability should not be discounted. We aimed to clarify the role of social group and matriline on FA, and thereby developmental stability, in female rhesus macaques. The Cayo Santiago macaques provide a unique opportunity to investigate the nuances of FA because of the wealth of information about the lives and deaths of each individual from the island. Further, in most cases, female rhesus macaques remain in the social group they were born into for their entire lives. We hypothesized that individuals in the same social group would exhibit similar levels of FA because they occupy similar geographical territory and are more closely related than females between social groups. Additionally, we hypothesized that individuals from higher ranking social groups will exhibit less FA than other social groups due to greater access to resources. Lastly, we hypothesized that individuals in the same matriline would exhibit more similar levels of FA to one another than other matrilines. We calculated craniofacial FA using 3D geometric morphometric techniques for 112 female macaques with known matrilines, 77 of which had known social groups. We used ANOVAs to compare mean FA between social groups and matrilines. No significantly different FA levels were observed between either (p=0.398 and p=0.752, respectively). These results indicate that genetic influence via relatedness may not have an impact on FA levels in a population and/or that FA is not distributed by social group or social group rank (though individual rank cannot be ruled out here). This work contributes to the FA literature by further parsing out the environmental and genetic influences affecting developmental instability.

Genetic studies on the Cayo Santiago rhesus macaques: A review of 40 years of research.

Genetic studies not only contribute substantially to our current understanding of the natural variation in behavior and health in many species, they also provide the basis of numerous in vivo models of human traits. Despite the many challenges posed by the high level of biological and social complexity, a long lifespan and difficult access in the field, genetic studies of primates are particularly rewarding because of the close evolutionary relatedness of these species to humans. The free-ranging rhesus macaque (Macaca mulatta) population on Cayo Santiago (CS), Puerto Rico, provides a unique resource in this respect because several of the abovementioned caveats are of either minor importance there, or lacking altogether, thereby allowing long-term genetic research in a primate population under constant surveillance since 1956. This review summarizes more than 40 years of genetic research carried out on CS, from early blood group typing and the genetic characterization of skeletal material via population-wide paternity testing with DNA fingerprints and short tandem repeats (STRs) to the analysis of the highly polymorphic DQB1 locus within the major histocompatibility complex (MHC). The results of the paternity studies also facilitated subsequent studies of male dominance and other factors influencing male reproductive success, of male reproductive skew, paternal kin bias, and mechanisms of paternal kin recognition. More recently, the CS macaques have been the subjects of functional genetic and gene expression analyses and have played an important role in behavioral and quantitative genetic studies. In addition, the CS colony has been used as a natural model for human adult-onset macular degeneration, glaucoma, and circadian rhythm disorder. Our review finishes off with a discussion of potential future directions of research on CS, including the transition from STRs to single nucleotide polymorphism (SNP) typing and whole genome sequencing.

The ticking clock of Cayo Santiago macaques and its implications for understanding human circadian rhythm disorders.

The circadian clock disorders in humans remain poorly understood. However, their impact on the development and progression of major human conditions, from cancer to insomnia, metabolic or mental illness becomes increasingly apparent. Addressing human circadian disorders in animal models is, in part, complicated by inverse temporal relationship between the core clock and specific physiological or behavioral processes in diurnal and nocturnal animals. Major advantages of a macaque model for translational circadian research, as a diurnal vertebrate phylogenetically close to humans, are further emphasized by the discovery of the first familial circadian disorder in non‐human primates among the rhesus monkeys originating from Cayo Santiago. The remarkable similarity of their pathological phenotypes to human Delayed Sleep Phase Disorder (DSPD), high penetrance of the disorder within one branch of the colony and the large number of animals available provide outstanding opportunities for studying the mechanisms of circadian disorders, their impact on other pathological conditions, and for the development of novel and effective treatment strategies. Am. J. Primatol. 78:117–126, 2016. © 2016 The Authors. American Journal of Primatology published by Wiley Periodicals, Inc.

What cortisol can tell us about the costs of sociality and reproduction among free-ranging rhesus macaque females on Cayo Santiago.

Research with the rhesus macaque population on Cayo Santiago can provide a unique perspective on the costs of sociality and reproduction in primates. Because the Cayo macaques live in unusually large groups and in a predator-free environment, in which their artificial food source lacks seasonal variation in abundance or quality, these monkeys constitute a semi-experimental study of the costs and benefits of group living. Here we review several long- and short-term studies that have focused on female life history and stress physiology. Long-term demographic data have shown that rhesus macaque females of middle- and low-ranking matrilines have lower adult survival probabilities than females of high-ranking matrilines. Costs of reproductive effort are also evident: adult females were more likely to die during the birth than during the mating season and they experienced higher cortisol levels when lactating. Lower-ranking females, in particular, experienced greater relative increase in cortisol production during lactation, in comparison to middle- and high-ranking females. Older high-ranking females had lower plasma cortisol levels than younger ones but cortisol levels were similarly high among young and old middle- and low-ranking females. Higher plasma cortisol levels and/or fecal glucocorticoid concentrations are associated with higher plasma concentrations of some proinflammatory cytokines. High cortisol, in turn, may be associated with chronic inflammation, and perhaps also with immunosuppression. In sum, the studies reviewed here provide multiple lines of evidence that sociality and reproductive effort impose measurable costs on female rhesus macaques. In line with socio-ecological theory, female dominance rank consistently emerges as an important modulator of variation in female life histories and physiology. The Cayo Santiago macaques are therefore a valuable model for elucidating the mechanisms by which within-group competition and reproduction impact health and survival in nonhuman primates and in humans.

Brief Communication: Linear enamel hypoplasia and the shift from irregular to regular provisioning in Cayo Santiago rhesus monkeys (Macaca mulatta)

This study investigates changes in the prevalence of linear enamel hypoplasia (LEH) before and after the shift from irregular to regular provisioning in the Cayo Santiago rhesus monkey population. Prior to 1956, monkeys on this island colony did not receive consistent provisions, and were reported to be in poor health (Rawlins and Kessler [1986] The Cayo Santiago Macaques; Albany: State University of New York Press). A regular provisioning program, instituted in August 1956, resulted in the improved health of individuals and the growth of the population (Rawlins and Kessler [1986] The Cayo Santiago Macaques; Albany: State University of New York Press). LEH, a developmental defect of enamel, is a sensitive indicator of systemic physiological stress (Goodman and Rose [1990] Yrbk. Phys. Anthropol. 33:59-110). It was therefore hypothesized that the prevalence of LEH would be higher in monkeys who were irregularly provisioned than in monkeys who experienced regular provisioning. To test this hypothesis, teeth were examined for LEH in a sample of 181 female rhesus monkeys. The results support the hypothesis: the mean number of defects was statistically significantly higher in the preprovisioned group than it was in the postprovisioned one. When LEH prevalence was assessed using only defects occurring on antimeric pairs, the preprovisioned group again had a higher prevalence than the postprovisioned one, although the difference was not statistically significant, most likely because of the reduced sample size. The results of this study indicate that changes in LEH prevalence, at least in this population of rhesus monkeys, are associated with changes in nutritional status.

Skeletal survey of Cayo Santiago rhesus macaques:osteoarthritis and articular plate excrescences

Objectives: This study was performed to complement studies on spondyloarthropathyin rhesus macaques by quantifying and characterizing another major form of arthritis and contrasting it with osteoarthritis. Methods: Skeletons of 269 macaques of known age and troop affiliation from the free-ranging Cayo Santiago colony (Caribbean Primate Research Center) were macroscopically surveyed for the presence of articular changes of osteoarthritis, articular plate excrescences, and calcifications that project back over the joint surface in all diarthrodial joints. Statistical tests were used to establish the independence of pathological conditions, age, gender, troop membership, and specific joint involvement. Results: Subchondral articular surface excrescences or calcific plate-like articular surface overgrowth were noted in 17% and osteoarthritis in 18% of Cayo Santiago macaques. Distribution of joint involvement and sex ratio (1:1) of the former condition were independent of either troop membership or the distribution of osteoarthritis. Conclusion: Three major forms of arthritis are common in rhesus macaques:osteoarthritis, spondyloarthropathy, and a category that might be referred to as apical plate excrescences (APE). The latter is very different from spondyloarthropathy, rheumatoid arthritis, osteoarthritis, gout, and infectious arthritis. It is quite similar to what in the past has been referred to as the radiographic form of calcium pyrophosphate deposition disease (CPPD) in humans. A new name has not been offered for the identification/categorization of this phenomenon in dry bone. Its occurrence in rhesus macaques appears to present a natural model for characterization of genetic, immunologic, and environmental aspects of this phenomenon. The acronym APE is offered for consideration in naming this category of arthritis in skeletal material.

Diurnal Intraocular Pressure Curves in Healthy Rhesus Macaques (Macaca mulatta) and Rhesus Macaques With Normotensive and Hypertensive Primary Open-Angle Glaucoma

The authors identify any diurnal intraocular pressure (IOP) variation in healthy Cayo Santiago macaques, as well as Cayo Santiago macaques with normotensive and hypertensive primary open-angle glaucoma (POAG), to further evaluate their potential value as a model for human POAG. Twenty-four monkeys (eight animals each of the healthy control, normotensive glaucoma, and hypertensive glaucoma groups) were sedated with ketamine hydrochloride and the IOP measured hourly from 8:00 AM until 3:00 PM with a Tonopen XL applanation tonometer (Mentor, Norwell, MA, U.S.A.). Mean IOP time profiles, mean IOPs at each observation time, and linear trends in mean IOP over time were compared among groups. Intraocular pressure rate-of-change over time and residual variation about the regression line for each individual eye were analyzed. Cup/disc ratio (C/D) was compared with baseline IOP, IOP profile mean and slope, and IOP residual variation. A significant group and time effect on mean IOP (p = 0.0001 and 0.011, respectively), with highest values at 2:00 PM or 3:00 PM, and a significant increasing linear trend in mean IOP over time in the hypertensive group were observed (p = 0.012). Intermediate readings between control and hypertensive mean IOPs were identified for the normotensive glaucoma group. The biggest range of IOP variation was found in the hypertensive glaucoma monkeys. Higher variations in IOP did not lead to an increase in C/D. This study provides evidence that the Cayo Santiago macaques are a valuable model for human normotensive and hypertensive POAG.

“Macaque‐ology” on a Caribbean Island. A review of the Cayo Santiago macaques: History, behavior and biology, edited by Richard G. Rawlins and Matt J. Kessler. Albany, State University of New York Press, 1986, 306 pp., $49.50 (cloth), $18.95 (paper)

“Macaque‐ology” on a Caribbean Island. A review of <i>the Cayo Santiago macaques: History, behavior and biology</i>, edited by Richard G. Rawlins and Matt J. Kessler. Albany, State University of New York Press, 1986, 306 pp., $49.50 (cloth), $18.95 (paper)

Leptospiral agglutinins in the Cayo Santiago macaques.

The colony of free-ranging rhesus monkeys (Macaca mulatta) on Cayo Santiago, Puerto Rico, was surveyed for leptospiral agglutinins. Only 5 (3%) of 169 monkeys (25% of the population) were seropositive (titers of ⩾ 1:100). An additional 29 animals (17%) had titers ⩽1:50. The proportions of seropositive males and females were 22% and 18%, respectively, and twice as many adult as immature animals (32% vs. 15%) were positive. In most seropositive monkeys a single serogroup predominated, Icterohaemorrhagiae being recorded in nearly 60% of these animals. In a follow-up survey conducted a year later, 4% of 158 of the original monkeys were seropositive, with titers of from 1:100 to 1:200. None of 22 Rattus rattus captured on Cayo Santiago had agglutinins to pathogenic serovars. Despite contact with rats and ingestion of stagnant water, the serological evidence, the excellent clinical condition, low mortality, and high reproductive rates of the Cayo Santiago macaques indicate that leptospirosis is not a health problem in this free ranging monkey colony.

The Cayo Santiago Macaques: History, behavior and biology. Edited by R. C. Rawlins and M. J. Kessler

The Cayo Santiago Macaques: History, behavior and biology. Edited by R. C. Rawlins and M. J. Kessler

Climate and seasonal reproduction in the Cayo Santiago macaques.

This paper reports the results of an eight-year study of seasonal reproduction in the free-ranging colony of rhesus monkeys on Cayo Santiago, Puerto Rico. There was a significant correlation between the start of the annual spring rainy season and the estimated median conception date (r = .94, p < .001) and median birth date (r = .94, p < .001). Conceptions followed the commencement of spring rains by 70 days. Significant and negative correlations were found between the number of days from the start of the rains to the first conception (r = -.93, p < 0.01) and median conceptions (r = -.91, p < .01). When spring rains were delayed, the interval between the onset of rains and conceptions decreased linearly. The median birth date for the Cayo Santiago population was accurately predicted for 1984 using two methods. When results from Cayo Santiago were applied retrospectively to data from the colony of rhesus monkeys near La Parguera, Puerto Rico, it explained the three-month difference in seasonality of reproduction between the two populations located at the same latitude (18°N). Photoperiod, as a function of latitude, appears to set the temporal limits of seasonal reproduction in rhesus macaques, while the onset of spring rains regulates reproductive activity within that range, at least in the Cayo Santiago population. The biological channel through which the effect is mediated has not been identified.

Nasal and cutaneous anatrichosomiasis in the free-ranging rhesus monkeys (Macaca mulatta) of Cayo Santiago.

One hundred and twenty-nine free-ranging rhesus monkeys on the island of Cayo Santiago were surveyed for the nematode Anatrichosoma cutaneum. The purpose of the study was to determine the prevalence of the nasal and cutaneous forms of this parasite in untreated rhesus monkeys maintained in a seminatural subtropical environment. The average prevalence of the nasal form in the sampled Cayo Santiago macaques was 23.2%. Adults were more commoly effected than yearling monkeys with 31.2% and 12.8% parasitized, respectively. Newborn infants were negative. No cases of the cutaneous form were identified. This study determined that nasal Anatrichosomiasis is common in the Cayo Santiago macaques. Further studies are necessary to establish the roles of intermediate host(s) and rhesus monkey behavior in the life cycle of this parasite in order to determine how Anatrichosomiasis has persisted for over 40 years in this colony.

Genetic studies of serum transferrins of free-ranging rhesus macaques of Cayo Santiago, Macaca mulatta (Zimmerman 1780).

AbstractTransferrin phenotypes of plasma from 687 semi‐free‐ranging Macaca mulatta living on Cayo Santiago, Puerto Rico, were determined by starch‐gel electrophoresis and autoradiography. Fifteen phenotypes, homozygous or heterozygous products of six codominant autosomal alleles, were present in the population. The 687 animals, prior to March 1973, were divided into eight troops plus peripheral males. By March 1, 1973 the size of the population was reduced to 333 animals, consisting of four troops plus peripheral males. The distributions of transferrin phenotypes and allele frequencies were determined for the population of 687 animals and for 287 of the March 1973 population of 333 animals. Gametic ratios of 382 offspring of 126 females were enumerated. Statistical tests of homogeneity and equilibrium were applied to the data. The results of these tests suggest that, with only a few exceptions, the Cayo Santiago macaques, although divided into social groups, form a single population, and the results are in accord with behavioral observations. The authors suggest that the data on transferrins provide a good baseline for future genetic and ethological studies of evolutionary processes in a population of nonhuman primates.