Primate Species Research Articles

Abstract B111: Population genetics identifies distinct subsets of prostate cancer risk variants between men of European, African and East Asian ancestry

Abstract Introduction Genome-wide association studies (GWAS) have identified Single Nucleotide Polymorphisms (SNPs) or variants associated with prostate cancer risk. The contribution of human genetic variation to racial disparities in prostate cancer is still not clearly understood. Men of African ancestry have the highest risk of prostate cancer, followed by European ancestry and lowest in men with East Asian ancestry. Prostate cancer is the most common cancer in human males, but non-human large primates do not develop prostate cancer naturally. This study investigated the population genetics of prostate cancer SNPs to identify those that were unique to ancestral groups, and also comparative genomics of human risk alleles and orthologous alleles in primates. Methods Prostate cancer SNPs were obtained from previous GWAS studies in the GWAS Catalog (https://www.ebi.ac.uk/gwas/home), and the GWAS Diversity Monitor Database (https://gwasdiversitymonitor.com). SNPs identified from discovery stages in AFR and EAS populations were included even when they did not replicate in EUR populations. Using Ensemble Release 109 (https://www.ensembl.org), the risk allele frequencies (RAF) in European (EUR), African (AFR) and East Asian (EAS) populations were obtained from the 1000 Genomes project and other population genetics data available on Ensembl. Population RAFs were used to identify variants that were present in only one ancestral group and not shared by other ancestral groups. A SNP was considered unique to a population if it was present in >1% of that population, but present in <.01% of the others. The risk alleles in Homo sapiens were compared to the orthologous ancestral primate allele using genome alignments from 10 primate species. Results 520 prostate cancer-associated SNPs were identified. 484 were shared between EUR, AFR and EAS populations. 10 SNPs were unique to EUR (on chromosomes 1, 2, 5, 8, 11, 17, 21, 22), 19 to AFR (on chromosomes 1, 5, 6, 8, 13, 17, 22) and 7 to EAS (on chromosomes 2, 10, 12, 13) populations. The gene sets involved by these SNPs were different in each ancestral group, with some overlap between EUR and AFR genes sets, but no overlap with the EAS genes set. The risk allele for all the 36 SNPs that were unique to EUR, AFR or EAS populations was different from the ancestral primate allele. Conclusion Prostate cancer SNPs unique to EUR, AFR and EAS populations were identified and are likely to be driving the genetic component of prostate cancer racial disparities. The genes involved were different between populations, which could have biological consequences and lead to distinct cancer phenotypes in men from different ancestral groups. The unique SNPs all had alleles different from the ancestral primate allele, suggesting that these variants emerged after human speciation and ‘Out of Africa’ human migration events. Citation Format: Chidi N. Molokwu, Evi O. Useh, Suresh Venugopal. Population genetics identifies distinct subsets of prostate cancer risk variants between men of European, African and East Asian ancestry [abstract]. In: Proceedings of the 16th AACR Conference on the Science of Cancer Health Disparities in Racial/Ethnic Minorities and the Medically Underserved; 2023 Sep 29-Oct 2;Orlando, FL. Philadelphia (PA): AACR; Cancer Epidemiol Biomarkers Prev 2023;32(12 Suppl):Abstract nr B111.

Simian immunodeficiency virus and storage buffer: Field-friendly preservation methods for RNA viral detection in primate feces.

Simian immunodeficiency virus (SIV), which originated in African monkeys, crossed the species barrier into humans and ultimately gave rise to HIV and the global HIV/AIDS epidemic. While SIV infects over 40 primate species in sub-Saharan Africa, testing for RNA viruses in wild primate populations can be challenging. Optimizing field-friendly methods for assessing viral presence/abundance in non-invasively collected biological samples facilitates the study of viruses, including potentially zoonotic viruses, in wild primate populations. This study compares SIV RNA preservation and recovery from non-human primate feces stored in four different buffers. Our results will inform future fieldwork and facilitate improved approaches to characterizing prevalence, shedding, and transmission of RNA viruses like SIV in natural hosts including wild-living non-human primates.

Cross-species amplification from non-human primate DNAs in commercial human DNA assay kits

Species specificity of commercial human DNA quantification kits and short tandem repeat (STR) profiling kits was examined using primate DNA samples. These samples comprised 33 individuals from eight primate species, each with gender and kinship data, including human (Homo sapiens), chimpanzee (Pan troglodytes), gorilla (Gorilla gorilla), and orangutan (Pongo pygmaeus) of Hominidae family, and Japanese macaque (Macaca fuscata), long-tailed macaque (Macaca fascicularis), hamadryas baboon (Papio hamadryas), and savannah monkey (Chlorocebus sp.) of Cercopithecidae family. The findings revealed varying levels of cross-species amplifications in all non-human DNA samples that correlated with their evolutionary proximity to humans, both kit types. Moreover, cross-species amplification, including female DNA samples, was observed in a Y-chromosomal STR profiling kit. Additionally, species specificity differed among the commercial kits examined. The cross-species amplification data presented in this study offer valuable assistance in interpreting the results of individual human identification in forensic cases involving non-human primates.

Assessment of habitat fragmentation impact on community taboo species for adoption as conservation portfolios in lowland rainforest ecological zone of Delta State, Nigeria

This study examined the impact of forest loss by fragmentation along four communities that taboo the species of primates and reptiles. Data by survey at three sighting regimes in a3×2×5 factorial experiments were square root-transformed before the analysis of variance and significant means separated at 5% level of probability with the Duncan multiple range tests. The fineness/coarseness of forest corridors and edges, availability of propagules and a-subjective habitat-matrix score for 7 key attributes of forest fragmentation along with soil samples analyzed for CEC, exchangeable cations and Ca-Mg ratio. Results showed higher mean population sighted in corridors than that of the edges. Propagule availability was Ugili Amai-Olloh Ossisa (18.5 kg/ha) >Ugono-Orogun (16.8 kg/ha)>Umute-Nsukwa (15.2 kg/ha)>Emu Uno (10.8 kg/ha) and underpinned intact fragment as Umute-Nsukwa>Ugili-Ossisa>Ugono-Orogu> Emu-Uno for the protection of IUCN Red List vulnerable white-throated guenon (Cercopithecus erythrogaster) and threatened West African dwarf crocodile (Osteollaemus tetraspis). Biodivers. Conserv. Bioresour. Manag. 2023, 9(2): 29-38

Evolutionary Patterns of Intersexual Power

Dominance and leverage are both possible causes of social inequality. If sexual dimorphism influences patterns of intersexual dominance, we predicted that highly dimorphic species are constrained to exhibit male-biased power (MP), but species with low sexual dimorphism are free to demonstrate a broader range of intersexual power relationships. If market effects influence intersexual leverage, we predicted that females have more power when group composition is more male-biased and estrus is asynchronous. We analyzed data on intersexual power, sexual dimorphism, expected estrous overlap, and sex ratio for 79 extant primate species using phylogenetic logistic regression and ancestral state reconstructions. Although MP is more common, every major primate clade includes non-MP species. MP was associated with greater body mass and canine length dimorphism and with female-biased sex-ratios. Low estrous overlap was associated with non-MP. Although MP was reconstructed as likely ancestral for anthropoids, the last common ancestor of this clade probably did not exhibit high sexual dimorphism. The last common ancestor of catarrhines was probably highly dimorphic, potentially constraining intersexual power relationships. Non-MP probably evolved multiple times in primates and may be less common because multiple traits are linked to MP while fewer traits are associated with female-biased power or equality.

ELOA3: A primate-specific RNA polymerase II elongation factor encoded by a tandem repeat gene cluster.

The biological role of the repetitive DNA sequences in the human genome remains an outstanding question. Recent long-read human genome assemblies have allowed us to identify a function for one of these repetitive regions. We have uncovered a tandem array of conserved primate-specific retrogenes encoding the protein Elongin A3 (ELOA3), a homolog of the RNA polymerase II (RNAPII) elongation factor Elongin A (ELOA). Our genomic analysis shows that the ELOA3 gene cluster is conserved among primates and the number of ELOA3 gene repeats is variable in the human population and across primate species. Moreover, the gene cluster has undergone concerted evolution and homogenization within primates. Our biochemical studies show that ELOA3 functions as a promoter-associated RNAPII pause-release elongation factor with distinct biochemical and functional features from its ancestral homolog, ELOA. We propose that the ELOA3 gene cluster has evolved to fulfil a transcriptional regulatory function unique to the primate lineage that can be targeted to regulate cellular hyperproliferation.

Phylogenetic comparative analysis of the cerebello-cerebral system in 34 species highlights primate-general expansion of cerebellar crura I-II

The reciprocal connections between the cerebellum and the cerebrum have been suggested to simultaneously play a role in brain size increase and to support a broad array of brain functions in primates. The cerebello-cerebral system has undergone marked functionally relevant reorganization. In particular, the lateral cerebellar lobules crura I-II (the ansiform) have been suggested to be expanded in hominoids. Here, we manually segmented 63 cerebella (34 primate species; 9 infraorders) and 30 ansiforms (13 species; 8 infraorders) to understand how their volumes have evolved over the primate lineage. Together, our analyses support proportional cerebellar-cerebral scaling, whereas ansiforms have expanded faster than the cerebellum and cerebrum. We did not find different scaling between strepsirrhines and haplorhines, nor between apes and non-apes. In sum, our study shows primate-general structural reorganization of the ansiform, relative to the cerebello-cerebral system, which is relevant for specialized brain functions in an evolutionary context.

Nutritional and Possible Pharmaceutical Aspects of Tree Exudates Eaten by Lemurs of Madagascar’s Dry Forests

Gums produced by trees after injuries are valuable food resources for several primate species. Yet, information on the chemical characteristics of gum is scant and inconsistent. We use gums consumed by lemurs (strepsirrhine primates of Madagascar) as an example to illustrate their possible nutritive and pharmaceutical properties. Exudates from 45 tree species of the dry forests of Madagascar contained 0.38–23.29% protein, 0.46–65.62% sugar, and 0.39–11.86 kJ/g of energy in dry matter. Exemplified by the lemur species Microcebus griseorufus, gum consumption increased with increasing sugar and energy content but was unrelated to protein. But lemurs also fed on gum with very low protein and energy content, suggesting that these exudates were consumed for other reasons. Disk diffusion tests with exudates from five out of 22 tree species consumed by lemurs showed antibacterial activity against Micrococcus spp. and/or Staphylococcus aureus. Exudates with antibacterial activity had lower protein, sugar, and energy contents than samples without antibacterial properties. GC-MS analyses revealed several components with antimicrobial effects that would have the potential for self-medication. This might explain the consumption of gum with very low nutritive value. Possible medicinal effects of tree exudates deserve further attention in view of their pharmaceutical applicability for animals and humans alike.

Eat the fruit earlier: Sakis (Pithecia chrysocephala) show enhanced temporal fruit resource access compared with squirrel monkeys (Saimiri sciureus) in an urban forest fragment in Brazil.

Fruit availability experienced by different primate species is likely to vary due to species-specific fruit use, even within the same habitat and timeframe. Pitheciines, primates of the subfamily Pitheciinae, particularly favor the seeds of unripe fruits. Researchers consider this dietary characteristic an adaptation to increase access to fruit resources. However, the relative advantages of pitheciines over sympatric non-pitheciine non-seed-eating primates regarding species-specific fruit availability is not well studied. In a 26-ha forest within the city of Manaus, Amazonian Brazil, we assessed the wild-food feeding behavior of free-ranging groups of golden-faced sakis (Pithecia chrysocephala) and sympatric common squirrel monkeys (Saimiri sciureus). We hypothesized that sakis would have greater and more consistent access to wild fruit due to (1) a wider variety of fruit species in their diet, and (2) longer consumption periods per fruit species. We recorded the plant species, part (pulp or seed), and developmental stage (ripe or unripe) of wild fruit consumed by both species. We also conducted monthly fruit censuses of 1000 trees and vines to estimate overall wild fruit abundance. As an indicator of fruit availability, we calculated the proportion of available fruiting trees and vines for each primate species separately based on their observed diet. Throughout the year, the proportion of available trees and vines was significantly higher and more temporally stable for sakis than for squirrel monkeys. This was because sakis used shared fruit species longer than squirrel monkeys by consuming both ripe and unripe fruit. Although sakis had a broader fruit repertoire than squirrel monkeys, it did not contribute to the higher fruit availability. Thus, the fruit feeding system of sakis identifies aspects of a niche that is less restricted in the timing of fruit consumption, which led to a relative advantage in fruit availability.

Food Composition and Preference of Captive Javan Langur (Trachypithecus auratus) in Gembira Loka Zoo, Yogyakarta

Javan langur (Trachypithecus auratus) is one of the endemic primate species of Indonesia. Its populations were exposed to extinction risk caused by human activities. Thus, conservation efforts such as ex-situ conservation were needed to preserve this species. One of the javan langur ex-situ conservation in Yogyakarta is the Gembira Loka Zoo. In captivity, animals must be guaranteed to be free from hunger and stay nourished. One aspect to support this welfare is food supply. Therefore, this study aimed to identify the food composition and analyze the correlation between food preference and feeding duration of each food item group. We used scan animal sampling method with five minutes intervals to observe the behavior of seven individuals of captive javan langurs. The result showed that there are three groups of food (fruit, vegetable, and leaf) provided daily to javan langurs in Gembira Loka Zoo. All the individuals spent most their time to consumed food from vegetable group, except for infant female who had the highest duration in the leaf group. In addition, based on which food they consumed first every feeding time (preference food), javan langurs preferred vegetable over fruit and leaf. Based on the Spearman correlation test, there are positive correlations of duration and preference of feeding except for leaf groups. This result was different from the natural food composition of javan langurs which mostly consisted of leaves. This study might help the zoo to consider the food items provided for the animals to increase animal welfare.

New records of the white-cheeked macaque provide range extension for the endangered primate in Gaoligong Mountains.

White-cheeked macaque Macaca leucogenys is a recently described primate species discovered by camera-trap surveys in the Medog region in 2015. The species was thought to be narrowly distributed in southeastern Tibet. However, knowledge on the distribution and conservation of the species is quite limited. Based on a systematic camera-trapping survey, we report the occurrence of the species in the Gaoligong Mountains, over 350km southeast of the nearest known population. We recorded 3025 photographs of white-cheeked macaques representing 481 independent records from 59 camera-trap stations with total trapping efforts of 18,437 camera days. Notably, part of the newly discovered locations of the white-cheeked macaque are outside of nature reserves without any formal protection and management. Our survey also confirms the occurrence of ten primate species in the Gaoligong Mountains, accounting for 35.7% of China's primates, including the Skywalker hoolock gibbon Hoolock tianxing and the Myanmar snub-nosed monkey Rhinopithecus strykeri etc. These findings reveal a new distribution record for the white-cheeked macaque and further highlight the conservation values of Gaoligong Mountains for globally threatened primate species. We also provide a preliminary report on the daily activity patterns of this endangered species, which enriches the bio-ecological data of the poorly studied species. We believe the report has significant implications for understanding the ecology of the species and improving conservation planning.

Assessment of the Population Status of Three Primate Species in Jaibui Island, Pujehun District, Southern Sierra Leone

Assessment of the Population Status of Three Primate Species in Jaibui Island, Pujehun District, Southern Sierra Leone

Activity Budget and Sociality of the Northern Lesser Galago, Galago senegalensis

AbstractComplex sociality in primates often is argued to have evolved after the appearance of diurnal activity. Studying the behaviour of nocturnal primates is fundamental to understanding the evolutionary origins of primate behaviour and ecology, yet much less is known about the nature of sociality in nocturnal primate species than their diurnal counterparts. We investigated group size, communication, and social interactions in free-ranging, Northern lesser galagos (Galago senegalensis) and present an activity budget and assessment of temporal variation in their behaviour. We collected continuous behavioural data using focal follows at three different stages of the night from individuals at Kwakuchinja, Northern Tanzania. We also collected group size data from Northern lesser galagos at Fongoli, Southeastern Senegal, and Lolldaiga Hills Ranch, Central Kenya. We categorised behaviours and, where sample sizes permitted, used Kruskal–Wallis tests to compare the durations of observed behaviours between the morning (pre-dawn), evening (from dusk), and later in the night. We analysed 140 focal follows (31.4 h of continuous behavioural data) and found that the proportion of time spent foraging, inactive, in locomotion, in self-maintenance, and vigilant, varied across the three stages of the night; galagos spent a great deal of their time inactive in the morning and foraging was more prevalent in the evening. Group size at Kwakuchinja was significantly larger than at Fongoli or LHR. Galagos were in groups of two or more in the majority of encounters at Kwakuchinja (55%; N = 76), rather than alone, but spent most of their nighttime activity alone at Fongoli (79%; N = 185) and LHR (80%; N = 142). Overall vocalisation rates were higher in the morning than other times throughout the night, although contact calls were relatively more frequent in the evening than other times. We recorded both affiliative and agonistic social interactions, but these contributed almost nothing to the overall activity budget. Our preliminary investigation into the social structure of Northern lesser galagos suggests that there are population differences in sociality and that overall, they connect more through vocalisations than through direct social interactions, thereby avoiding some of the potential costs associated with group-living. This variation in social organization suggests that we have more to learn about the drivers of sociality in nocturnal primates and the nature of their social structure.

Immunogenicity and Efficacy of TNX-1800, A Live Virus Recombinant Poxvirus Vaccine Candidate, against SARS-CoV-2 Challenge in Nonhuman Primates.

TNX-1800 is a synthetically derived live recombinant chimeric horsepox virus (rcHPXV) vaccine candidate expressing Wuhan SARS-CoV-2 spike (S) protein. The primary objective of this study was to evaluate the immunogenicity and efficacy of TNX-1800 in two nonhuman primate species challenged with USA-WA1/2020 SARS-CoV-2. TNX-1800 vaccination was well tolerated with no serious adverse events or significant changes in clinical parameters. A single dose of TNX-1800 generated humoral responses in African Green Monkeys and Cynomolgus Macaques, as measured by the total binding of anti-SARS-CoV-2 S IgG and neutralizing antibody titers against the USA-WA1/2020 strain. In addition, a single dose of TNX-1800 induced an interferon-gamma (IFN-γ)-mediated T-cell response in Cynomolgus Macaques. Following challenge with SARS-CoV-2, African Green and Cynomolgus Macaques exhibited rapid clearance of virus in the upper and lower respiratory tract. Future studies will assess the efficacy of TNX-1800 against newly emerging variants and demonstrate its safety in humans.

Frontal mechanisms underlying primate calls recognition by humans.

The ability to process verbal language seems unique to humans and relies not only on semantics but on other forms of communication such as affective vocalizations, that we share with other primate species-particularly great apes (Hominidae). To better understand these processes at the behavioral and brain level, we asked human participants to categorize vocalizations of four primate species including human, great apes (chimpanzee and bonobo), and monkey (rhesus macaque) during MRI acquisition. Classification was above chance level for all species but bonobo vocalizations. Imaging analyses were computed using a participant-specific, trial-by-trial fitted probability categorization value in a model-based style of data analysis. Model-based analyses revealed the implication of the bilateral orbitofrontal cortex and inferior frontal gyrus pars triangularis (IFGtri) respectively correlating and anti-correlating with the fitted probability of accurate species classification. Further conjunction analyses revealed enhanced activity in a sub-area of the left IFGtri specifically for the accurate classification of chimpanzee calls compared to human voices. Our data-that are controlled for acoustic variability between species-therefore reveal distinct frontal mechanisms that shed light on how the human brain evolved to process vocal signals.

A map of white matter tracts in a lesser ape, the lar gibbon

The recent development of methods for constructing directly comparable white matter atlases in primate brains from diffusion MRI allows us to probe specializations unique to humans, great apes, and other primate taxa. Here, we constructed the first white matter atlas of a lesser ape using an ex vivo diffusion-weighted scan of a brain from a young adult (5.5 years) male lar gibbon. We find that white matter architecture of the gibbon temporal lobe suggests specializations that are reminiscent of those previously reported for great apes, specifically, the expansion of the arcuate fasciculus and the inferior longitudinal fasciculus in the temporal lobe. Our findings suggest these white matter expansions into the temporal lobe were present in the last common ancestor to hominoids approximately 16 million years ago and were further modified in the great ape and human lineages. White matter atlases provide a useful resource for identifying neuroanatomical differences and similarities between humans and other primate species and provide insight into the evolutionary variation and stasis of brain organization.

Is sugar as sweet to the palate as seeds are appetizing to the belly? Taste responsiveness to five food-associated carbohydrates in zoo-housed white-faced sakis, Pithecia pithecia.

Differences in taste perception between species are thought to reflect evolutionary adaptations to dietary specialization. White-faced sakis (Pithecia pithecia) are commonly considered as frugivores but are unusual among primates as they do not serve as seed dispersers but rather prey upon the seeds of the fruits they consume and are thought to exploit the lipids and proteins that these seeds contain in high amounts. Using a two-bottle preference test of short duration we therefore assessed whether this dietary specialization affects the taste responsiveness of four adult white-faced sakis for five food-associated carbohydrates. We found that the sakis significantly preferred concentrations as low as 10 mM sucrose, 10-40 mM fructose, 20-30 mM glucose and maltose, and 30-40 mM lactose over tap water. When given the choice between all binary combinations of these five saccharides presented at equimolar concentrations of 100, 200, and 300 mM, respectively, the sakis displayed significant preferences for individual saccharides in the following order: sucrose > fructose > glucose ≥ maltose = lactose. These results demonstrate that seed-predating white-faced sakis have a well-developed taste sensitivity for food-associated carbohydrates which is not inferior to that of most other primates including seed-dispersing frugivores, but rather ranks among the more sweet-taste sensitive species. Further, they show that their pattern of relative preference for the five carbohydrates is similar to that found in other frugivorous primate species. These findings may represent an example of Liem's paradox as the sakis' morphological adaptations to efficiently predate on and exploit the lipid- and protein-rich hard-shelled seeds of fruits does not compromise their ability to detect the carbohydrates found in the pulp of fruits at low concentrations.

A conceptual framework for assessing behavioral flexibility of species in response to extreme climatic events

Inherent differences in the adaptive capacity of species to flexibly respond to extreme climatic events (ECEs) represent a key factor in their survivorship. We introduce and apply a conceptual framework linking knowledge about species’ current ecology and biology with variation in behavioral flexibility to ECEs. We applied it to 199 non-human primate species currently exposed to cyclones across the global tropics. Our findings suggest that species characterized by an increased ability to exploit a broad range of food types, social systems that permit subgrouping, and habitat types that span a range of environmental conditions may have greater success in coping with cyclones than more narrowly constrained or less adaptable primates. Overall, 15% of species, predominantly of the families Atelidae and Cercopithecidae, were assessed as having high or very high flexibility. In contrast, ~ 60% of primates were assessed with low or very low flexibility. These were species mainly belonging to the Cheirogaleidae, Lemuridae, Lepilemuridae, and Indriidae. While much work remains to better understand mechanisms driving differences in behavioral flexibility of species exposed to extreme climate across vertebrate lineages, our framework provides a workable approach that can improve estimates of current vulnerability to these phenomena and better inform conservation and management strategies.

Evolutionary scaling and cognitive correlates of primate frontal cortex microstructure.

Investigating evolutionary changes in frontal cortex microstructure is crucial to understanding how modifications of neuron and axon distributions contribute to phylogenetic variation in cognition. In the present study, we characterized microstructural components of dorsolateral prefrontal cortex, orbitofrontal cortex, and primary motor cortex from 14 primate species using measurements of neuropil fraction and immunohistochemical markers for fast-spiking inhibitory interneurons, large pyramidal projection neuron subtypes, serotonergic innervation, and dopaminergic innervation. Results revealed that the rate of evolutionary change was similar across these microstructural variables, except for neuropil fraction, which evolves more slowly and displays the strongest correlation with brain size. We also found that neuropil fraction in orbitofrontal cortex layers V-VI was associated with cross-species variation in performance on experimental tasks that measure self-control. These findings provide insight into the evolutionary reorganization of the primate frontal cortex in relation to brain size scaling and its association with cognitive processes.

Human and Non-Human Primate Coexistence in Argentina: Conflicts and Solutions.

There are five different primate species inhabiting widely distinct ecoregions in Argentina. Each of them faces various threats in terms of conservation and conflicts that hamper their ability to coexist with human populations. We present here some of the drivers known to be the causes of conflicts between humans and primates in the southernmost area of distribution of Latin American primates. We focus our synthesis on two of the biggest sources of conflict: the effects of different anthropogenic disturbances, and human misconceptions concerning the role of primates in the ecosystem. In each section, we briefly characterize the conflicts worldwide and then provide specific cases and examples from Argentina. In the last part of the manuscript, we further describe some ongoing national and regional educational, research, and conservation approaches to mitigate those effects.