The reverse zoonotic potential of SARS-CoV-2.

There has been considerable emphasis recently on the zoonotic origins of emerging infectious diseases in humans, including the SARS-CoV-2 pandemic; however, reverse zoonoses (infections transmitted from humans to other animals) have received less attention despite their potential importance. The effects can be devastating for the infected species and can also result in transmission of the pathogen back to human populations or other animals either in the original form or as a variant. Humans have transmitted SARS-CoV-2 to other animals, and the virus is able to circulate and evolve in those species. As global travel resumes, the potential of SARS-CoV-2 as a reverse zoonosis threatens humans and endangered species. Nonhuman primates are of particular concern given their susceptibility to human respiratory infections. Enforcing safety measures for all people working in and visiting wildlife areas, especially those with nonhuman primates, and increasing access to safety measures for people living near protected areas that are home to nonhuman primates will help mitigate reverse zoonotic transmission.

Facial and genital color ornamentation, testosterone, and reproductive output in high-ranking male rhesus macaques.

Males in many vertebrate species have colorful ornaments that evolved by sexual selection. The role of androgens in the genesis and maintenance of these signals is unclear. We studied 21 adult high-ranking male rhesus macaques from nine social groups in the free-ranging population on Cayo Santiago, Puerto Rico, and analyzed facial and genital skin luminance and redness, fecal androgens, rates of mating behaviors, and offspring sired. Facial and genital coloration varied in relation to age, mating behavior, reproductive success, and testosterone concentration. Our results indicate that skin coloration in high-ranking male rhesus macaques is a sexually-selected trait mediated by androgens. These results add to the growing literature on the proximate and ultimate causes of male sexual signals and highlight the need to examine how these characteristics change with age in other species.

Male-philopatric nonhuman primates and their potential role in understanding the evolution of human sociality.

In most primate species, males transfer out of their natal groups, resulting in groups of unrelated males. However, in a few species, including humans, males remain in their groups and form life-long associations with each other. This pattern of male philopatry is linked with cooperative male behaviors, including border patrols and predator defense. Because females in male-philopatric species form weaker kin networks with each other than in female-philopatric species, they are expected to evolve counter-strategies to male sexual coercion that are relatively independent of support from other females. Studies of male-philopatric nonhuman primates can provide insight into the evolutionary basis of prosocial behaviors, cooperation, and group action in humans and offer comparative models for understanding the sociality of other hominin species. This review will discuss patterns of dispersal and philopatry across primates, explore the resulting male and female behaviors, and argue that male-philopatric nonhuman primate species offer insight into the social and sexual dynamics of hominins throughout evolution.

Differences in sperm morphology between Alouatta palliata and Alouatta pigra are consistent with the intensity of sperm competition in each species.

The intensity of sperm competition, in which sperm compete within the female reproductive tract to reach and fertilize her eggs, varies in species with different mating systems. Sperm competition is more intense in species where males cannot monopolize access to reproductive females and females mate with multiple males. In this scenario, a morphological change that increases the ability of sperm to reach and fertilize eggs should rapidly spread in the population, leading to sperm morphological differences between closely related species. Differences in sperm morphology have been reported among primate species with different mating systems. However, due to the inherent logistical and ethical difficulties to sample sperm from wild primates, the extent of variation in sperm morphology within species and among closely related species remains understudied. Here, we compared sperm morphological traits from two sister howler monkey species (Alouatta palliata and Alouatta pigra) that have different mating systems to investigate the effect of sperm competition on sperm morphological traits. We predicted that sperm from A. palliata, where females have more opportunities to mate with multiple males, would show differences in traits associated with increase sperm competitiveness compared to A. pigra where females mostly mate with the central male. We used linear mixed models to determine species differences in sperm morphology, controlling for individual variation. We found that midpieces and heads in A. palliata sperm were on average 26.2% and 11.0% longer, respectively, than those of A. pigra. Differences in these traits are important for sperm speed and hydrodynamic movement in other species and can affect fertilization success. This study provides empirical evidence of sperm morphological traits that evolved through sexual selection in sister primate species with different mating systems.

Validation of a method for quantifying urinary C-peptide in platyrrhine monkeys.

Urinary C-peptide (UCP) is a biomarker for insulin that can be used as a non-invasive physiological measure of energy balance. Previous research has validated the use of UCP to quantify energy balance in catarrhines; however, there have been no such studies in platyrrhines. Validation is necessary in this lineage of primates as divergent evolution has resulted in varied organization of insulin genes. Here, we evaluate a method for quantifying UCP in platyrrhines to measure energetic expenditure, a key component of calculating energy balance. Urine samples were opportunistically collected from laboratory-housed tufted capuchins (Sapajus apella) during exercise activities. To examine the efficacy of using UCP as a means for assessing energetic condition, we analyzed urine samples collected before and after exercise. Urinary C-peptide concentrations were measured using a commercial C-peptide radioimmunoassay. We found that on average, UCP concentrations were 0.34 ng/mL lower after exercise than they were prior to exercise (range =0.04 to 0.71 ng/mL). The rateofenergy expenditureper unit time was greater when capuchins were exercising at faster speeds. Concordantly, UCP concentrations decreased more following exercise at those faster speeds. Parallelism of serial dilutions of samples was calculated to assess the precision of UCP concentrations produced using these methods. Measured UCP concentrations decreased at expected intervals in accordance with each dilution factor. Our results provide biological validation of the use of a commercial assay for quantifying UCP as a measure of energy expenditure in this platyrrhine species.

Age negatively impacts reproduction in high-ranking male rhesus macaques on Cayo Santiago, Puerto Rico.

Based on sexual selection theory, the reproductive potential of male primates is expected to be limited by access to fertile females. Alpha males, the highest ranking males in a social group, are predicted to have better access to mates and produce more offspring until they are no longer dominant, which usually corresponds with age. Little is known about male reproductive senescence independent of rank changes in nonhuman primates. Here, we examine variation in the reproductive success of high-ranking male rhesus macaques on Cayo Santiago. We recorded behavioral data for 21 adult males across 9 social groups during the 2013 mating season. Additionally, we used paternity data from the long-term database to determine the number of offspring each subject sired over his lifetime and during the study period. Older high-ranking males in stable groups had fewer offspring than younger high-ranking males in stable groups in 2013. The low reproductive output for the older males was not a result of lower mating effort, and reproductive output in 2013 was not predicted by total prior reproductive success. Our results provide novel evidence of post-copulatory reproductive senescence in high-ranking male nonhuman primates.

Methods for detecting Zika virus in feces: A case study in captive squirrel monkeys (Saimiri boliviensis boliviensis).

A strain of Zika virus (ZIKV) of Asian origin associated with birth defects and neurological disorders has emerged and spread through the Americas. ZIKV was first isolated in the blood of nonhuman primates in Africa and has been detected in the blood, saliva, and urine of a few catarrhine species in both Africa and Asia, suggesting that nonhuman primates may serve as both a source and a reservoir of the virus. The recent introduction of ZIKV to human populations in the Americas presents the potential for the virus to spread into nonhuman primate reservoirs. Thus, it is critical to develop efficient and noninvasive detection methods to monitor the spread of the virus in wild nonhuman primate populations. Here, we describe a method for ZIKV detection in noninvasively collected fecal samples of a Neotropical primate. Fecal samples were collected from two captive squirrel monkeys (Saimiri boliviensis boliviensis) that were experimentally infected with ZIKV (Strain Mexico_1_44) and an additional two uninfected squirrel monkeys. Nucleic acids were extracted from these samples, and RT-qPCR was used to assay for the presence of ZIKV using primers flanking a 101 bp region of the NS5 gene. In both ZIKV-inoculated animals, ZIKV was detected 5-11 days post-infection, but was not detected in the uninfected animals. We compare the fecal results to ZIKV detection in serum, saliva, and urine samples from the same individuals. Our results indicate that fecal detection is a cost-effective, noninvasive method for monitoring wild populations of Neotropical primates as possible ZIKV reservoirs.

Demography and life history of a group of white-bellied spider monkeys (Ateles belzebuth) in western Amazonia.

Species-specific demographic parameters and life history variables are important for understanding how individual primate taxa have adapted to evolutionary and ecological pressures and for conducting interspecific comparisons as well as for conducting population viability analyses and for managing captive populations. Here, we describe results from a 12+ year study of the demographic dynamics of a wild group of white-bellied spider monkeys (Ateles belzebuth belzebuth) living near the Tiputini Biodiversity Station in a largely pristine rainforest in western Amazonia. Across the study period, group size varied between 25 and 37 individuals, and there was a clearly female-biased sex ratio within all age classes. Females were the dispersing sex, as 19 females born into the group disappeared close to reaching adult body size and were presumed to have emigrated, while seven subadult or adult females joined the group during the study period. We estimated the age of dispersal for females at 5.9 ± SD 0.4 years (N = 13). Our study confirms that males are the philopatric sex, as all natal males have remained in the group and some have begun to reproduce, while no males have immigrated. Males began ranging independently from their mothers at ∼4.5 years of age and began copulating with adult females by the age of ∼5 years. Females had long inter-birth intervals (44.2 ± SD 7.8 months; range: 32-64 months, N = 21). Based on our data, female spider monkeys might have longer life spans than males, as only one out of six adult males but 9 out of 11 adult females present in the group in mid 2005 were still present in January 2018. The slow development and extended life histories of wild spider monkeys pose significant challenges for the ability of these primates to cope with habitat degradation and hunting throughout their geographical distribution.

Alpha male status and availability of conceptive females are associated with high glucocorticoid concentrations in high-ranking male rhesus macaques (Macaca mulatta) during the mating season.

The relationship between male mating opportunities, stress, and glucocorticoid concentrations is complicated by the fact that physiological stress and glucocorticoid concentrations can be influenced by dominance rank, group size, and the stability of the male dominance hierarchy, along with ecological factors. We studied the three highest-ranking males in nine different social groups within the same free-ranging population of rhesus macaques on Cayo Santiago, Puerto Rico, during the mating season, to examine variation in glucocorticoid concentrations in relation to number of females that conceived each month, alpha status, number of adult males in a group, and male rank hierarchy stability. We found that glucocorticoid concentrations were highest in the early mating season period when more females conceived in each group and declined linearly as the mating season progressed and the number of conceptive females decreased. Alpha males had significantly higher mean monthly glucocorticoid concentrations than other high-ranking males throughout the study period. Male age, number of adult males in a group, and hierarchy stability were not significantly associated with glucocorticoid concentrations. Our findings suggest that alpha males may experience significantly higher levels of physiological stress than their immediate subordinates and that this stress coincides with the period of the mating season when most conceptions occur.

Links between breast cancer and birth weight: an empirical test of the hypothesized association between size at birth and premenopausal adult progesterone concentrations.

Some studies have reported that birth size is a risk factor for breast cancer, but the reasons for this observation are unknown. Ovarian hormone concentrations may be a link between birth size and breast cancer, but the few tests of this hypothesis are inconsistent, perhaps because of differences in sample composition, inclusion of anovulatory cycles, or use of one hormonal measurement per woman. We present results from the first study to use daily hormonal measurements throughout a woman's complete ovulatory cycle to test the hypothesized relationship between birth size and adult progesterone concentrations. We used a study sample and accompanying data set previously obtained for another research project in which we had collected daily urine samples from 63 healthy premenopausal women throughout a menstrual cycle. Multivariate regression was used to test for trends of individual progesterone indices (from 55 ovulatory cycles) with birth weight or ponderal index, while controlling for age, adult BMI, and age at menarche. Our main finding was that neither birth weight nor ponderal index was associated with biologically significant variation in luteal progesterone indices; the best-estimated effect sizes of birth size on these progesterone indices were small (3.7-10.2%). BMI was the only significant predictor of mean peak urinary progesterone, but it explained <6% of the variance. Our findings, in light of what is currently known regarding associations of breast cancer risk with birth size and adult size, suggest that environmental factors (particularly those that vary by socioeconomic status and affect growth) may underlie associations between birth size and cancer risks without there being any association of birth size with adult ovarian hormone concentrations.

Female red colobus monkeys maintain their densities through flexible feeding strategies in logged forests in Kibale National Park, Uganda.

Behavioral flexibility allows primates to cope with environmental variability. Quantifying primate responses to human habitat modifications allows an effective means of assessing coping mechanisms. Within Kibale National Park, Uganda, logging led to reduced primate food availability that still exists almost 50 years after the harvest. Following the predictions of the ideal free distribution theory, primate densities are expected to decrease in areas of lower resource availability so that the resources available per individual are equivalent in logged and old-growth areas. However, counter to what would be predicted by the ideal free distribution theory, red colobus monkeys (Procolobus rufomitratus) occur at similar densities in logged and old-growth areas of Kibale. This suggests that either the ecological differences between the two areas are not sufficient to impact red colobus densities or that animals in logged areas are compensating to changes in resource availability by using different foraging strategies. To test between these hypotheses, we examined four groups of red colobus, two in logged and two in old-growth forests, and compared feeding behavior, feeding tree size, and tree productivity. Females in logged areas fed on resources from a greater number of plant species, fed on fewer resources from each species, and spent more time feeding than those in old-growth areas. By expanding their diet, females in logged areas effectively increased the resources available to them, which may contribute to their ability to maintain similar densities to females in old-growth areas. These findings have implications for an evolutionary understanding of how species deal with environmental change and considerations for conservation practices that determine what areas should be prioritized for protection.

Sexual conflict in primates.

Sexual conflict is increasingly recognized as a major force for evolutionary change and holds great potential for delineating variation in primate behavior and morphology. The goals of this review are to highlight the rapidly rising field of sexual conflict and the ongoing shift in our understanding of interactions between the sexes. We discuss the evidence for sexual conflict within the Order Primates, and assess how studies of primates have illuminated and can continue to increase our understanding of sexual conflict and sexual selection. Finally, we introduce a framework for understanding the behavioral, anatomical, and genetic expression of sexual conflict across primate mating systems and suggest directions for future research.