Elizabeth Maldonado

Sex differences in survival costs of reproduction in a promiscuous primate

In sexually promiscuous mammals, female reproductive effort is mainly expressed through gestation, lactation, and maternal care, whereas male reproductive effort is mainly manifested as mating effort. In this study, we investigated whether reproduction has significant survival costs for a seasonally breeding, sexually promiscuous species, the rhesus macaque, and whether these costs occur at different times of the year for females and males, namely in the birth and the mating season, respectively. The study was conducted with the rhesus macaque population on Cayo Santiago, Puerto Rico. Data on 7,402 births and 922 deaths over a 45-year period were analyzed. Births were concentrated between November and April, while conceptions occurred between May and October. As predicted, female mortality probability peaked in the birth season whereas male mortality probability peaked in the mating season. Furthermore, as the onset of the birth season gradually shifted over the years in relation to climatic changes, there was a concomitant shift in the seasonal peaks of male and female mortality. Taken together, our findings provide the first evidence of sex differences in the survival costs of reproduction in nonhuman primates and suggest that reproduction has significant fitness costs even in environments with abundant food and absence of predation.

Prevalence of human immunodeficiency virus-associated cognitive impairment in a group of Hispanic women at risk for neurological impairment.

Human immunodeficiency virus (HIV)-associated cognitive impairment, a significant cause of morbidity, affects up to 30% of HIV-infected people. Its prevalence doubled as patients began to live longer after the introduction of highly active retroviral therapy. Women are now one of the fastest growing groups with acquired immunodeficiency syndrome (AIDS) in the United States and Puerto Rico, but relatively little is known about the prevalence and characteristics of cognitive dysfunction in HIV-infected women. In this study the authors investigated its prevalence in a group of HIV-1—seropositive Hispanic women in Puerto Rico. Forty-nine women with a nadir CD4 cell count of ≤500 cells/mm3 were enrolled. Cognitive impairment was defined according to the American Academy of Neurology criteria for HIV dementia as modified to identify an “asymptomatic cognitively impaired” group. Observed prevalence was compared with prevalence in other populations in United States, Europe, and Australia. Differences in clinical markers and neuropsychological test performance among the cohort stratified by cognitive impairment were tested. Cognitive impairment was observed in 77.6% (38/49) of cases; asymptomatic cognitive impairment in 32.7% (16/49); minor cognitive motor disorders in 16.3% (8/49); and HIV-associated dementia (HAD) in 28.6% (14/49). Cognitive impairment did not correlate with age, CD4 cell count, viral load, or treatment modality. The cross-sectional prevalence of HIV-associated cognitive impairment was 77.6% (28.6% for HAD). These findings should enhance awareness of the prevalence of HIV-associated cognitive impairment, both clinically apparent and “asymptomatic,” in Hispanic women and lead to improvements in areas such as education and compliance and to reevaluation of treatment interventions.

Associations of cigarette smoking with viral immune and cognitive function in human immunodeficiency virus–seropositive women

Cigarette smoking alters the immune system and may improve cognitive deficits in neuropsychiatric disorders. Smoking prevalence is high in human immunodeficiency virus (HIV)—infected patients; however, its effect on HIV-associated cognitive impairment remains unknown in the era of antiretroviral treatment. The authors examined associations of smoking with viral immune profile and cognitive function in a cohort of HIV-seropositive women. This observational cross-sectional study included 56 women (36 HIV-seropositive and 20 HIV-seronegative) surveyed with a tobacco questionnaire: the Fagerström Test for Nicotine Dependency. Viral immune status was obtained 6 to 12 months before questioned. Neurocognitive testing (NP) assessed verbal memory, frontal/executive function, psychomotor speed, and motor speed. A reference group of HIV-seronegative women was used to calculate standardized z-scores. Cognitive impairment was classified using a modified American Academy of Neurology criteria, adding an asymptomatic group based on NP tests. Statistics included parametric and nonparametric tests. HIV-seropositive women were more likely to report a history of smoking (P = 0.028). Among them, current smoking correlated with higher plasma viral load (P = 0.048), and history of smoking correlated with lower CD4 cell count (P = 0.027). The authors observed no associations between cognitive impairment and either current or past history of smoking and no differences in neurocognitive domain scores between HIV-seropositive and -seronegative women or between those with and without a history of smoking. However, restricting analysis to HIV-seropositives showed a significant better performance on the frontal/executive domain in those with history of smoking. In summary, history of smoking correlated with better frontal/executive cognitive domain performance in HIV-seropositive women and with worse viral immune profile.

Breaking the succession rule: the costs and benefits of an alpha-status take-over by an immigrant rhesus macaque on Cayo Santiago

Explaining intraspecific variation in reproductive tactics hinges on measuring associated costs and benefits. Yet, this is difficult if alternative (purportedly less optimal) tactics remain unobserved. We describe a rare alpha-position take-over by an immigrant male rhesus macaque in a population where males typically gain rank via succession. Unusually, male aggressiveness after the take-over correlated with rank and mating success. The new alpha achieved the highest mating and reproductive success. Nevertheless, he sired only 4 infants due to high extra-group paternity (59.3%). The costs of his immigration tactic were high: after the mating season ended, unable to deter coalitionary attacks by resident males, he was overthrown. The following year he had the highest relative annual weight loss and levels of immune activation among males in the group. Succession-based rank-acquisition in large, provisioned groups of macaques thus appears to be actively maintained by resident males, who impose high costs on challengers.

Translational spatial task and its relationship to HIV-associated neurocognitive disorders and apolipoprotein e in HIV-seropositive women

HIV-associated neurocognitive disorders (HAND) continue to be a neurological complication of HIV infection in the era of combined antiretroviral therapy. Hippocampal neurodegeneration and dysfunction occurs as a result of HIV infection, but few studies to date have assesses spatial learning and memory function in patients with HAND. We used the Memory Island (MI) test to study the effects of HIV infection, apolipoprotein E (ApoE) allele status, and cerebral spinal fluid (CSF) ApoE protein levels on spatial learning and memory in our cohort of Hispanic women. The MI test is a virtual reality-based computer program that tests spatial learning and memory and was designed to resemble the Morris Water Maze test of hippocampal function widely used in rodent studies. In the current study, HIV-seropositive women (n = 20) and controls (n = 16) were evaluated with neuropsychological (NP) tests, the MI test, ApoE, and CSF ApoE assays. On the MI, the HIV-seropositive group showed significant reduced learning and delayed memory performance compared with HIV-seronegative controls. When stratified by cognitive performance on NP tests, the HIV-seropositive, cognitively impaired group performed worse than HIV-seronegative controls in ability to learn and in the delayed memory trial. Interestingly, differences were observed in the results obtained by the NP tests and the MI test for ε4 carriers and noncarriers: NP tests showed effects of the ε4 allele in HIV-seronegative women but not HIV-seropositive ones, whereas the converse was true for the MI test. Our findings suggest that the MI test is sensitive in detecting spatial deficits in HIV-seropositive women and that these deficits may arise relatively early in the course of HAND.

Familial periodontal disease in the cayo santiago rhesus macaques

Substantial ongoing research continues to explore the contribution of genetics and environment to the onset, extent and severity of periodontal disease(s). Existing evidence supports that periodontal disease appears to have an increased prevalence in family units with a member having aggressive periodontitis. We have been using the nonhuman primate as a model of periodontal disease for over 25 years with these species demonstrating naturally occurring periodontal disease that increases with age. This report details our findings from evaluation of periodontal disease in skulls from 97 animals (5–31 years of age) derived from the skeletons of the rhesus monkeys (Macaca mulatta) on Cayo Santiago. Periodontal disease was evaluated by determining the distance from the base of the alveolar bone defect to the cemento‐enamel junction on 1st/2nd premolars and 1st/2nd molars from all four quadrants. The results demonstrated an increasing extent and severity of periodontitis with aging across the population of animals beyond only compensatory eruption. Importantly, irrespective of age, extensive heterogeneity in disease expression was observed among the animals. Linking these variations to multi‐generational matriarchal family units supported familial susceptibility of periodontitis. As the current generations of animals that are descendants from these matrilines are alive, studies can be conducted to explore an array of underlying factors that could account for susceptibility or resistance to periodontal disease. Am. J. Primatol. 78:143–151, 2016.

Herpes B-virus seroreactivity in a colony of Macaca mulatta: data from the Sabana Seca Field Station, a new specific pathogen-free program.

Abstract:  The demand for B‐virus‐free animals for biomedical research is increasing, while at the same time the availability of such animals is decreasing. The establishment of Specific Pathogen‐Free (SPF) breeding macaque colonies is a priority of the National Institutes of Health. Nevertheless, it is well known that seroreactivity to B‐virus can be difficult to interpret, particularly as it can vary over time in a single animal. The aim of the present study was to implement a reliable algorithm to examine B‐virus reactivity among the rhesus monkey population of the Caribbean Primate Research Center. The sensitivity and specificity of our assay were determined using reports from two different laboratories as references. Whereas 95.4% of animals showed consistent serological status and 4.6% of animals recruited to this SPF program showed serovariability to B‐virus over the initial 2 years of examination. Implications for all SPF programs are discussed in this article.

Differential distribution of antibodies to different viruses in young animals in the free-ranging rhesus macaques of Cayo Santiago

Background  The breeding colony of free‐ranging rhesus macaques was established in 1938 in Cayo Santiago (CS) with animals collected in northern India. The seroprevalence to cercopithecine herpesvirus type 1 (B virus) and simian retroviruses has been studied previously.

Managing the Cayo Santiago rhesus macaque population: The role of density

Cayo Santiago is the oldest continuously operating free‐ranging rhesus monkey colony in the world. Population control of this colony has historically been carried out by periodic live capture and removal of animals. However, the effect of such a strategy on the size, growth rate, age structure, and sex ratio of the population has not been analyzed. This study reviews past removal data and uses a population projection model to simulate the effects of different removal schemes based on Cayo Santiago demographic data from 2000–2012. The model incorporates negative density‐dependence in female fertility, as well as male and female survival rates, to determine the population‐level effects of selective removal by age and sex. Modeling revealed that removal of sexually immature individuals has negligible effects on the population dynamics explaining why with an initial population of 1309 in 2000 and annual removals of immature monkeys a mean annual population growth rate of 12% and a final population size of ∼1,435 individuals by 2012 (∼0.009 animal/m2) was observed. With no removals, the population is expected to exhibit dampened oscillations until reaching equilibrium at ∼1,690 individuals (∼0.0111 animal/m2) in 2,100. In contrast, removal of adult females (≥4 yrs) would significantly reduce the population size, but would also promote an increase in population growth rate due to density feedback. A maximum annual production of 275 births is expected when 550 adult females are present in the population. Sensitivity analyses showed that removing females, in contrast to controlling their fertility through invasive treatments would contribute the most to changes in population growth rate. Given the density compensation on fertility, stabilizing the population would require removing ∼80% of the current population of adult females. This study highlights the importance of addressing the population‐level density effects, as well as sensitivity analyses, to optimize management strategies. Am. J. Primatol. 78:167–181, 2016.

Odontogenic Abscesses in Rhesus Macaques (Macaca mulatta) of Cayo Santiago

OBJECTIVES Odontogenic abscesses are one of the most common dental diseases causing maxillofacial skeletal lesions. They affect the individuals ability to maintain the dental structures necessary to obtain adequate nutrition for survival and reproduction. In this study, the prevalence and pattern of odontogenic abscesses in relation to age, sex, matriline, and living periods were investigated in adult rhesus macaque skeletons of the free-ranging colony on Cayo Santiago, Puerto Rico. MATERIALS AND METHODS The skulls used for this study were from the skeletons of 752 adult rhesus macaques, aged 8-31 years, and born between 1951 and 2000. They came from 66 matrilines ranging from 1 to 88 individuals. Fistulae or skeletal lesions caused by odontogenic abscesses drainage, carious lesions, tooth fractures, tooth loss, and alveolar resorption were evaluated visually. RESULTS Seventy-two specimens (9.57%) had odontogenic abscesses of varying severity. Males had a significantly higher prevalence than females. The prevalence of odontogenic abscesses in several matrilines was significantly higher than in the population as a whole. Animals born between 1950 and 1965 tended to have a higher prevalence of odontogenic abscesses than those born in later periods. DISCUSSION These results suggest that oral pathologies, such as dental and periodontal abscesses in rhesus macaques are fairly common, which may indicate familial effects interwoven with ecological and social factors. The closeness of the rhesus and human genomes allows insights to understand of the epidemiology of these diseases in the human population. Further assessment of the role played by environmental and familial factors on rhesus oral health and disease are warranted.