Rufomitratus Research Articles

Reciprocity and rotating social advantage among females in egalitarian primate societies

Interfemale competition regimes in primate societies have been described as despotic or egalitarian based on female social behaviour. Hierarchies and nepotism are typical of despotic primates, where dominance rank and kinship are known to be strong drivers of who grooms whom and who fights with whom. However, a general theory for what structures female–female interactions in egalitarian societies remains underdeveloped. We present two nonmutually exclusive hypotheses that each propose a mechanism for levelling social advantages in a group by conferring social favour to all or most females over time: transitory states (age, residency status and reproductive state) bias social interactions and/or reciprocity governs social interactions. In this study, we (1) determined that a group of red colobus monkeys, Procolobus rufomitratus tephrosceles, in Kibale National Park, Uganda, are highly egalitarian; (2) tested our hypotheses for how egalitarianism may be maintained in this group; and (3) analysed findings across primate studies for support for either hypothesis. In red colobus, agonistic interactions were predicted by age – a transitory state – and transitory states and reciprocity predicted grooming interactions: avid groomers, older females and short-term resident females received more grooming. In addition, behavioural indicators of social status (aggression given and grooming received) were not associated with reproductive success in red colobus, as might be expected in an egalitarian group where variance in fitness should be low. Across primates, we found that transitory states commonly structure social interactions in egalitarian societies but not in despotic societies and that reciprocity is highly variable, especially among egalitarian societies. Rotating social advantage as females shift among transitory states and/or reciprocate grooming may lower interfemale skew in social benefits and potentially in lifetime reproductive success in egalitarian groups, setting them apart from despotic societies where dominance hierarchies and kinship maintain a more static and unequal distribution of social advantage.

Spatial configuration becomes more important with increasing habitat loss: a simulation study of environmentally-transmitted parasites

Landscape changes can be an important modifier of disease. Habitat fragmentation commonly results in reduced connectivity in host populations and increased use of the remaining habitat. For environmentally transmitted parasites, this presents a possible trade-off between transmission potential at the local and global level. We quantify the effects of fragmentation on the transmission of an environmentally transmitted parasite, teasing apart the relative effects of habitat composition and configuration on both host movement behaviour and subsequent infection patterns. We use a spatially-explicit epidemiological model to simulate the effects of habitat fragmentation, using, as an example, whipworm (Trichuris sp.) within a red colobus monkey population (Procolobus rufomitratus). We found that habitat fragmentation did not always lead to a trade-off between population connectivity and concentration of habitat use in host movement behaviour or in final population infection patterns. However, our simulation results suggest the spatial configuration of the remaining habitat became increasingly influential on behavioural and infection outcomes as habitat was removed. Additionally, we found common fragmentation metrics provided little ability to explain variation in propagation of infections. Our results suggest an interaction between habitat configuration and composition should be considered when assessing disease related impacts of habitat fragmentation on environmentally transmitted parasites, especially in cases where habitat loss is high (≥ 30%). We also propose that spatially-explicit simulations that capture a host’s response to fragmentation could aid in the development of novel landscape metrics targeted towards specific host-parasite-landscape systems.

Cis-regulatory evolution in a wild primate: Infection-associated genetic variation drives differential expression of MHC-DQA1 invitro.

Few studies have combined genetic association analyses with functional characterization of infection-associated SNPs in natural populations of nonhuman primates. Here, we investigate the relationship between host genetic variation, parasitism and natural selection in a population of red colobus (Procolobus rufomitratus tephrosceles) in Kibale National Park, Uganda. We collected parasitological, cellular and genomic data to test the following hypotheses: (i) MHC-DQA1 regulatory genetic variation is associated with control of whipworm (Trichuris) infection in a natural population of red colobus; (ii) infection-associated SNPs are functional in driving differential gene expression invitro; and (iii) balancing selection has shaped patterns of variation in the MHC-DQA1 promoter. We identified two SNPs in the MHC-DQA1 promoter, both in transcription factor binding sites, and both of which are associated with decreased control of Trichuris infection. We characterized the function of both SNPs by testing differences in gene expression between the two alleles of each SNP in two mammalian cell lines. Alleles of one of the SNPs drove differential gene expression in both cell lines, while the other SNP drove differences in expression in one of the cell lines. Additionally, we found evidence of balancing selection acting on the MHC-DQA1 promoter, including extensive trans-species polymorphisms between red colobus and other primates, and an excess of intermediate-frequency alleles relative to genome-wide, coding and noncoding RADseq data. Our data suggest that balancing selection provides adaptive regulatory flexibility that outweighs the consequences of increased parasite infection intensity in heterozygotes.

Spatial patterns of persistence for environmentally transmitted parasites: Effects of regional climate and local landscape

Both regional climatic conditions and local landscape characteristics can affect the ability of environmentally transmitted parasites to persist outside their host. In general, implications of shifting climate conditions on the persistence and spread of parasites have been examined in the absence of interactions with local landscape characteristics (e.g., forest fragmentation). Here, we test the utility of a model that includes regional climate and local landscape characteristics to model environmental persistence of parasites. We used a system with both a well-studied landscape and data-rich host-parasite relationship and investigated how regional and local conditions affected the transmission of a parasitic whipworm (Trichuris spp.) within a population of red colobus monkeys (Procolobus rufomitratus) in Kibale National Park, Uganda. We model persistence of a whipworm deposit in the environment as a function of both regional climate suitability and its sensitivity to the local conditions in which it was deposited. Our simulation suggests that changes to regional climate suitability impacts prevalence patterns in hosts to a larger extent than sensitivity to local landscape characteristics, with no evidence of an interaction effect. However, we find that in landscapes that offer fewer suitable sites for egg persistence (i.e., high sensitivity to local landscape characteristics), our model predicts greater variability in parasite prevalence among host groups, and a shift to source-sink parasite dynamics. Our results suggest that when modeling environmentally-transmitted parasites, explicitly considering spatial patterns of environmental persistence and host movement behaviour provides insight into transmission dynamics of specific landscape-host-parasite systems.

Sickness behaviour associated with non-lethal infections in wild primates.

Non-lethal parasite infections are common in wildlife, but there is little information on their clinical consequences. Here, we pair infection data from a ubiquitous soil-transmitted helminth, the whipworm (genus Trichuris), with activity data from a habituated group of wild red colobus monkeys (Procolobus rufomitratus tephrosceles) in Kibale National Park, Uganda. We use mixed-effect models to examine the relationship between non-lethal parasitism and red colobus behaviour. Our results indicate that red colobus increased resting and decreased more energetically costly behaviours when shedding whipworm eggs in faeces. Temporal patterns of behaviour also changed, with individuals switching behaviour less frequently when whipworm-positive. Feeding frequency did not differ, but red colobus consumption of bark and two plant species from the genus Albizia, which are used locally in traditional medicines, significantly increased when animals were shedding whipworm eggs. These results suggest self-medicative plant use, although additional work is needed to verify this conclusion. Our results indicate sickness behaviours, which are considered an adaptive response by hosts during infection. Induction of sickness behaviour in turn suggests that these primates are clinically sensitive to non-lethal parasite infections.

Competing pressures on populations: long-term dynamics of food availability, food quality, disease, stress and animal abundance.

Despite strong links between sociality and fitness that ultimately affect the size of animal populations, the particular social and ecological factors that lead to endangerment are not well understood. Here, we synthesize approximately 25 years of data and present new analyses that highlight dynamics in forest composition, food availability, the nutritional quality of food, disease, physiological stress and population size of endangered folivorous red colobus monkeys (Procolobus rufomitratus). There is a decline in the quality of leaves 15 and 30 years following two previous studies in an undisturbed area of forest. The consumption of a low-quality diet in one month was associated with higher glucocorticoid levels in the subsequent month and stress levels in groups living in degraded forest fragments where diet was poor was more than twice those in forest groups. In contrast, forest composition has changed and when red colobus food availability was weighted by the protein-to-fibre ratio, which we have shown positively predicts folivore biomass, there was an increase in the availability of high-quality trees. Despite these changing social and ecological factors, the abundance of red colobus has remained stable, possibly through a combination of increasing group size and behavioural flexibility.

Genomic resources notes accepted 1 December 2014 - 31 January 2015.

This article documents the public availability of (i) transcriptome sequence data and assembly for the rostrum dace (Leuciscus burdigalensis) naturally infected by a copepod ectoparasite (Tracheliastes polycolpus) and (ii) SNPs identified and validated from RAD sequencing for the Ugandan red colobus (Procolobus rufomitratus tephrosceles) using RAD sequencing.

Group Size Dynamics over 15+ Years in an African Forest Primate Community

AbstractGroup size affects many aspects of the ecology and social organization of animals. We investigated group size stability for five primate species in Kibale National Park, Uganda from 1996 to 2011 at three nested spatial scales. Survey data indicated that group sizes did not change for most species, with the exception of red colobus monkeys (Procolobus rufomitratus), in which group size increased at all spatial scales. Mangabey (Lophocebus albigena) group size increased in old‐growth forest, but the sample size and increase were small. To augment this survey data, we collected several years of demographic data on three habituated groups of redtail monkeys (Cercopithecus ascanius), eight groups of black‐and‐white colobus (Colobus guereza), and one red colobus group. The red colobus group increased from 59 to 104 individuals, while redtail monkey and black‐and‐white colobus group sizes were stable, mirroring our survey results. To understand mechanisms behind group size changes in red colobus versus stability in other primates, we monitored forest dynamics at two spatial scales between 1990 and 2013, considered changes in predator population, and explored evidence of disease dynamics. The cumulative size of all trees and red colobus food trees increased over 24 yr, suggesting that changing food availability was driving group size changes for red colobus, while predation and disease played lesser roles. Overall, our results and evidence of changing primate densities suggest that the Kibale primate community is in a non‐equilibrium state. We suggest future conservation and management efforts take this into consideration.

How monkeys see a forest: genetic variation and population genetic structure of two forest primates

The biological traits of different species usually predispose them to dissimilar levels of extinction risk. Accordingly, we analysed genetic variation and population genetic structure of two endangered forest monkeys to determine how they were influenced by habitat change. The Tana River red colobus and mangabey are of similar body size, are sympatric and endemic to forests in Kenya. The mangabey is frugivorous, terrestrial and exhibits female philopatry but the colobus is folivorous, arboreal and both sexes exhibit natal dispersal. We predicted that both species would have low genetic variation due to high genetic drift, and possible inbreeding, because their populations are relatively small and subdivided in forest fragments. Nevertheless, we expected the mangabeys to have a higher genetic variation because they have a larger population, and their higher vagility would enhance gene flow. Thus, we expected a stronger population genetic structure in the colobus because lower vagility would constrain dispersal and increase genetic differentiation. Finally, we expected both species to exhibit isolation by distance due to greater gene flow among populations in close geographic proximity. We genotyped 146 colobus and 76 mangabeys with nine microsatellite markers and found that both species had relatively high heterozygosities but low allelic richness. Furthermore, allelic richness, heterozygosity and genetic differentiation were all higher in the mangabey and only the mangabey exhibited isolation by distance. Taken together, our results suggest that species with divergent behavioral ecologies may exhibit differential vulnerabilities to genetic erosion due to habitat change.

Increasing Group Size Alters Behavior of a Folivorous Primate

Group size influences many aspects of mammalian social life, including stress levels, disease transmission, reproductive rates, and behavior. However, much of what is known about the effects of group size on behavioral ecology has come from comparisons across multiple groups of different sizes. These findings may be biased because behavioral differences across groups may be more indicative of how environmental variation influences animal behavior, rather than group size itself. To partially circumvent this limitation, we used longitudinal data to examine how changes in group size across time affect the behavior of folivorous red colobus monkeys (Procolobus rufomitratus) of Kibale National Park, Uganda. Controlling for food availability, we demonstrated that increasing group size resulted in altered activity budgets, based on 6 yr of data on a group that increased from 57 to 98 members. Specifically, as group size increased, individuals spent less time feeding and socializing, more time traveling, and increased the diversity of their diet. These changes appear to allow the monkeys to compensate for greater scramble competition apparent at larger group sizes, as increasing group size did not show the predicted relationship with lower female fecundity. Our results support recent findings documenting feeding competition in folivorous primates. Our results also document behavioral flexibility, an important trait that allows many social mammals to maximize the benefits of sociality (e.g., increased vigilance), while minimizing the costs (e.g., increased feeding competition).

High genetic diversity and adaptive potential of two simian hemorrhagic fever viruses in a wild primate population.

Key biological properties such as high genetic diversity and high evolutionary rate enhance the potential of certain RNA viruses to adapt and emerge. Identifying viruses with these properties in their natural hosts could dramatically improve disease forecasting and surveillance. Recently, we discovered two novel members of the viral family Arteriviridae: simian hemorrhagic fever virus (SHFV)-krc1 and SHFV-krc2, infecting a single wild red colobus (Procolobus rufomitratus tephrosceles) in Kibale National Park, Uganda. Nearly nothing is known about the biological properties of SHFVs in nature, although the SHFV type strain, SHFV-LVR, has caused devastating outbreaks of viral hemorrhagic fever in captive macaques. Here we detected SHFV-krc1 and SHFV-krc2 in 40% and 47% of 60 wild red colobus tested, respectively. We found viral loads in excess of 106–107 RNA copies per milliliter of blood plasma for each of these viruses. SHFV-krc1 and SHFV-krc2 also showed high genetic diversity at both the inter- and intra-host levels. Analyses of synonymous and non-synonymous nucleotide diversity across viral genomes revealed patterns suggestive of positive selection in SHFV open reading frames (ORF) 5 (SHFV-krc2 only) and 7 (SHFV-krc1 and SHFV-krc2). Thus, these viruses share several important properties with some of the most rapidly evolving, emergent RNA viruses.

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.

Timing is everything: expanding the cost of sexual attraction hypothesis

Anthropogenic disturbances present challenges to animals. Behavioural plasticity is one way that animals adjust to degraded habitats. In the present study, we examined how ecological conditions impact reproduction of female red colobus monkeys, Procolobus rufomitratus, in Kibale National Park, Uganda. Wrangham (2002, Behavioural diversity in chimpanzees and bonobos, pp. 204–215) proposed the ‘cost of sexual attraction’ hypothesis to explain the relationship between ecology and female reproduction. Here for the first time we test and expand on this hypothesis in a folivorous species, the red colobus monkey. We compared four groups of red colobus, two in previously logged areas and two in old-growth areas, to examine differences in female reproductive behaviours and physiologies. We predicted that, because of differences in food availability, females living in logged areas would (1) have a shorter duration of genital tumescence, (2) mate less frequently and (3) constrain mating behaviours more to periods of maximal genital tumescence compared to females in old-growth areas. As predicted, females in logged areas were fully tumescent for a significantly shorter period, copulated significantly less frequently and showed mating behaviours when fully inflated significantly more than females in old-growth areas. This behavioural plasticity contributes to the maintenance of female reproductive function in the face of environmental constraints associated with anthropogenic disturbance that influences food resources.

Nodule worm infection in humans and wild primates in Uganda: cryptic species in a newly identified region of human transmission.

IntroductionSoil-transmitted helminths (STHs) are a major health concern in tropical and sub-tropical countries. Oesophagostomum infection is considered endemic to West Africa but has also been identified in Uganda, East Africa, among primates (including humans). However, the taxonomy and ecology of Oesophagostomum in Uganda have not been studied, except for in chimpanzees (Pan troglodytes), which are infected by both O. bifurcum and O. stephanostomum.Methods and FindingsWe studied Oesophagostomum in Uganda in a community of non-human primates that live in close proximity to humans. Prevalence estimates based on microscopy were lower than those based on polymerase chain reaction (PCR), indicating greater sensitivity of PCR. Prevalence varied among host species, with humans and red colobus (Procolobus rufomitratus) infected at lowest prevalence (25% and 41% by PCR, respectively), and chimpanzees, olive baboons (Papio anubis), and l'hoest monkeys (Cercopithecus lhoesti) infected at highest prevalence (100% by PCR in all three species). Phylogenetic regression showed that primates travelling further and in smaller groups are at greatest risk of infection. Molecular phylogenetic analyses revealed three cryptic clades of Oesophagostomum that were not distinguishable based on morphological characteristics of their eggs. Of these, the clade with the greatest host range had not previously been described genetically. This novel clade infects humans, as well as five other species of primates.ConclusionsMultiple cryptic forms of Oesophagostomum circulate in the people and primates of western Uganda, and parasite clades differ in host range and cross-species transmission potential. Our results expand knowledge about human Oesophagostomum infection beyond the West African countries of Togo and Ghana, where the parasite is a known public health concern. Oesophagostomum infection in humans may be common throughout Sub-Saharan Africa, and the transmission of this neglected STH among primates, including zoonotic transmission, may vary among host communities depending on their location and ecology.

Fecal microbiomes of non‐human primates in Western Uganda reveal species‐specific communities largely resistant to habitat perturbation

Primate gastrointestinal microbial communities are becoming increasingly appreciated for their relevance to comparative medicine and conservation, but the factors that structure primate "microbiomes" remain controversial. This study examined a community of primates in Kibale National Park, Uganda, to assess the relative importance of host species and location in structuring gastrointestinal microbiomes. Fecal samples were collected from primates in intact forest and from primates in highly disturbed forest fragments. People and livestock living nearby were also included, as was a geographically distant population of related red colobus in Kenya. A culture-free microbial community fingerprinting technique was used to analyze fecal microbiomes from 124 individual red colobus (Procolobus rufomitratus), 100 individual black-and-white colobus (Colobus guereza), 111 individual red-tailed guenons (Cercopithecus ascanius), 578 human volunteers, and 364 domestic animals, including cattle (Bos indicus and B. indicus × B. taurus crosses), goats (Caprus hircus), sheep (Ovis aries), and pigs (Sus scrofa). Microbiomes sorted strongly by host species, and forest fragmentation did not alter this pattern. Microbiomes of Kenyan red colobus sorted distinctly from microbiomes of Ugandan red colobus, but microbiomes from these two red colobus populations clustered more closely with each other than with any other species. Microbiomes from red colobus and black-and-white colobus were more differentiated than would be predicted by the phylogenetic relatedness of these two species, perhaps reflecting heretofore underappreciated differences in digestive physiology between the species. Within Kibale, social group membership influenced intra-specific variation among microbiomes. However, intra-specific variation was higher among primates in forest fragments than among primates in intact forest, perhaps reflecting the physical separation of fragments. These results suggest that, in this system, species-specific processes such as gastrointestinal physiology strongly structure microbial communities, and that primate microbiomes are relatively resistant to perturbation, even across large geographic distances or in the face of habitat disturbance.

Emergent group level navigation: an agent-based evaluation of movement patterns in a folivorous primate.

The foraging activity of many organisms reveal strategic movement patterns, showing efficient use of spatially distributed resources. The underlying mechanisms behind these movement patterns, such as the use of spatial memory, are topics of considerable debate. To augment existing evidence of spatial memory use in primates, we generated movement patterns from simulated primate agents with simple sensory and behavioral capabilities. We developed agents representing various hypotheses of memory use, and compared the movement patterns of simulated groups to those of an observed group of red colobus monkeys (Procolobus rufomitratus), testing for: the effects of memory type (Euclidian or landmark based), amount of memory retention, and the effects of social rules in making foraging choices at the scale of the group (independent or leader led). Our results indicate that red colobus movement patterns fit best with simulated groups that have landmark based memory and a follow the leader foraging strategy. Comparisons between simulated agents revealed that social rules had the greatest impact on a group’s step length, whereas the type of memory had the highest impact on a group’s path tortuosity and cohesion. Using simulation studies as experimental trials to test theories of spatial memory use allows the development of insight into the behavioral mechanisms behind animal movement, developing case-specific results, as well as general results informing how changes to perception and behavior influence movement patterns.

Physiological and Behavioral Effects of Capture Darting on Red Colobus Monkeys (Procolobus rufomitratus) with a Comparison to Chimpanzee (Pan troglodytes) Predation

Understanding how human activities affect wild primates is critical to the design of effective conservation strategies. Despite this need, few studies have examined the physiological and behavioral effects of field research methods in the wild. Here, we examine how the stress response, i.e., fecal cortisol, and behavior of Ugandan red colobus monkeys (Procolobus rufomitratus) in Kibale National Park are affected by chemical immobilization and collaring, i.e., capture. We compare this anthropogenic stressor to a naturally occurring stressor: a chimpanzee (Pan troglodytes) predation attack. Two adult males had peak cortisol levels of 283 and 284 ng/g 2–3 d after capture, which were 190% and 182% above their baseline levels, i.e., the first sample taken immediately after capture, but these peak levels did not remain elevated. Using long-term data, i.e., 11 mo of data, we found no difference in fecal cortisol levels between 10 darted and collared individuals and 14 individuals living in the same social group that were not darted or collared. For the chimpanzee attack, peak fecal cortisol levels (147–211% above baseline) were recorded 1–4 d after the attack, but these levels also did not remain elevated for long. These data show that darting and collaring and a chimpanzee predation attempt caused an acute stress response, but neither leads to sustained elevated cortisol levels. Thus, in situations in which research contributes significantly to the conservation of primates and cannot be conducted noninvasively, capture darting appears to be a useful technique with minimal long-term effects as long as injury and mortality are avoided. However, we encourage researchers to make similar physiological and behavioral comparisons in other field studies using similar techniques to provide a better understanding of the effects of research practices on the stress physiology and social behavior of wild primates.

Is Markhamia lutea’s abundance determined by animal foraging?

Understanding the determinants of tropical forest tree richness and spatial distribution is a central goal of forest ecology; however, the role of herbivorous mammals has received little attention. Here we explore the potential for red colobus monkeys (Procolobus rufomitratus) to influence the abundance of Markhamia lutea trees in a tropical forest by feeding extensively on the tree’s flowers, such that this tree population is not able to regularly set fruit. Using 14years of data from Kibale National Park, Uganda, we quantify M. lutea flower and fruit production. Similarly, using 21years of data, we quantify temporal changes in the abundance of stems in size classes from 1m tall and above. Our analyses demonstrate that M. lutea is rarely able to produce fruit and that this corresponds to a general decline in its abundance across all size classes. Moreover, using 7years of feeding records, we demonstrate that red colobus feed on M. lutea, consuming large amounts of leaf and flower buds whenever they were available, suggesting that this behavior limits fruit production. Therefore, we suggest that red colobus are presently important for structuring the distribution and abundance of M. lutea in Kibale. This dynamic raises the intriguing question of how a large M. lutea population was able to originally establish. There is no evidence of a change in red colobus population size; however, if this old-growth forest is in a non-equilibrium state, M. lutea may have become established when red colobus ate a different diet.

The Roles of Phytoestrogens in Primate Ecology and Evolution

Most primates depend heavily on plant foods; thus their chemical composition is key to understanding primate ecology and evolution. One class of plant compounds of strong current interest are phytoestrogens, which have the potential to alter fertility, fecundity, and survival. These plant compounds mimic the activity of vertebrate estrogens, resulting in altered physiology and behavior. Here, we review what is known about phytoestrogens from an ecological and evolutionary perspective. Much of what is known about the effects of phytoestrogens on the endocrine system comes from research on human foods, especially soybeans (Glycine max). Two opposing perspectives have resulted from this research: 1) phytoestrogens provide health benefits, such as cancer prevention, or 2) phytoestrogens act as endocrine disruptors and threaten reproductive health. Studies of wild primates have only recently begun examining the presence of estrogenic plants in the primate diet and the effects of their consumption. Evidence that a number of primate species eat plants containing phytoestrogens and research documenting behavioral and hormonal effects of estrogenic plant consumption for red colobus monkeys (Procolobus rufomitratus) augment captive and laboratory studies to suggest that these compounds promote differential survival and reproduction. Although much debate is currently taking place over the role of phytoestrogens and other endocrine disruptors in human health issues and in threatening biodiversity, we argue that an ecological and evolutionary approach is needed to reach appropriate conclusions.

Co-infection and cross-species transmission of divergent Hepatocystis lineages in a wild African primate community

Hemoparasites of the apicomplexan family Plasmodiidae include the etiological agents of malaria, as well as a suite of non-human primate parasites from which the human malaria agents evolved. Despite the significance of these parasites for global health, little information is available about their ecology in multi-host communities. Primates were investigated in Kibale National Park, Uganda, where ecological relationships among host species are well characterized. Blood samples were examined for parasites of the genera Plasmodium and Hepatocystis using microscopy and PCR targeting the parasite mitochondrial cytochrome b gene, followed by Sanger sequencing. To assess co-infection, “deep sequencing” of a variable region within cytochrome b was performed. Out of nine black-and-white colobus (Colobus guereza), one blue guenon (Cercopithecus mitis), five grey-cheeked mangabeys (Lophocebus albigena), 23 olive baboons (Papio anubis), 52 red colobus (Procolobus rufomitratus) and 12 red-tailed guenons (Cercopithecus ascanius), 79 infections (77.5%) were found, all of which were Hepatocystis spp. Sanger sequencing revealed 25 different parasite haplotypes that sorted phylogenetically into six species-specific but morphologically similar lineages. “Deep sequencing” revealed mixed-lineage co-infections in baboons and red colobus (41.7% and 64.7% of individuals, respectively) but not in other host species. One lineage infecting red colobus also infected baboons, but always as the minor variant, suggesting directional cross-species transmission. Hepatocystis parasites in this primate community are a diverse assemblage of cryptic lineages, some of which co-infect hosts and at least one of which can cross primate species barriers.