Individual, Social, and Environmental Factors Associated with Patterns of Parasitic Infection in Capuchin Monkeys (Cebus imitator)
Parasites, and the infectious diseases they carry, are thought to have significantly impacted our evolutionary trajectory for millennia. Exploring how parasites are acquired and transmitted by their hosts in wild, natural populations is integral to understanding how similar processes may have shaped host-parasite co-evolutionary relationships over time. However, parasitological studies in humans and in non-human primates have produced inconsistent results, highlighting the dynamic, nuanced, and unique relationships individual parasites have with their hosts. These relationships are largely regulated by variation in factors at host, social, and environmental levels. Characteristics unique to the host (e.g., age and sex), factors pertaining to aspects of host sociality (e.g., host group size, kinship, dominance rank, etc.), and environmental factors (e.g., climate and habitat composition) all work independently and in tandem to affect both a host’s chance of encountering a parasite and its susceptibility to infection by that parasite. In this dissertation, I integrate morphological and molecular methods in parasitology to explore how host-level, social, and environmental factors relate to patterns of gastrointestinal parasitic infection in wild capuchin monkeys (Cebus imitator) living in a highly seasonal tropical dry forest in Northwestern Costa Rica. In Chapter 1, I begin by reviewing the two main ‘pillars’ of parasitic infections: susceptibility and encounter. I then briefly review common, well-studied, and importantgastrointestinal parasites of non-human primates before explaining why non-human primates make useful models for studying human health and evolution. I follow by reviewing recent studies examining patterns of parasitism in non-human primates before introducing my model species, the white-faced capuchin. I end the chapter by providing a brief overview of my three major research questions, introducing this study’s field site and study population, and end by briefly explaining my sample collection and processing methods. Due to the majority of my sample and data collection occurring during the Covid-19 pandemic, the types and amount of data that could be collected for my dissertation were limited. To conclude, I highlight these limitations as well as the benefits of conducting research on long-studied host populations from well-known field sites. Chapter 2 reports the results of a study exploring the preservation efficacy of ethanol- and formalin-fixed fecal samples. The goal of this study was to determine if ethanol could be used as a viable fecal preservation medium for morphological parasite identification. If validated, this would offer opportunities to explore both morphological and molecular parasite diversity in the same samples simultaneously, a method not possible with formalin preserved samples. We collected 21 fecal samples from our study population and placed one half of the sample in 10% buffered neutral formalin, the other half in 96% ethanol. We then screened both halves of the samples for parasites using the same wet lab techniques. While we frequently found more egg and larval morphotypes in the formalin-preserved halves of the samples, we did not find any significant difference in the number of eggs and larvae recovered from samples preserved in either medium. Both ethanol and formalin somewhat distorted the morphological structure of larvae, but overall, ethanol was shown to be a suitable medium for the morphological identification of parasites in samples stored over one year at room temperature. I conceptualized,planned, and prepared the publication, while my undergraduate mentee, Joelle Hass, led the lab work and analyses with support from Jessica Churcher and Hadjira Hamou. Samples for this dissertation were collected by Suheidy Romero Morales and the rest of the Sector Santa Rosa Primate Project. In Chapter 3, I report how I use ethanol preserved samples to characterize the diversity of parasites found in my host population using both morphological and molecular methods. I first used microscopy to screen samples for endoparasites before collecting individual larvae from those samples for molecular identification using Sanger Sequencing of the ITS-2 genetic marker. I then explored how parasitic infections related to host age, sex, rank, social group, and season. I identified seven parasitic morphotypes in our samples and found that overall infection intensity increased with host age. Specifically, the infection intensity of Filariopsis sp., a highly prevalent, but understudied lungworm, also increased with host age, whereas the prevalence and infection intensity of Strongyloides sp., a soil-transmitted helminth known as a threadworm, decreased with host age. There were also host social group-level and seasonal differences in parasitic infections for several other parasites identified in our samples, including the tapeworm Hymenolepis sp. and subulurids. These findings suggest that the parasites identified in our samples may respond to variables on different ecological levels in different ways. They also produced opened up several interesting avenues of inquiry that I used to guide my future research (Chapters 3, 4, and 5). In addition to these results, I also generated the first genetic data for Filariopsis and found close genetic matches for larvae we were unable to identify using morphology alone. The generated molecular data complemented and deepened our understanding of our previously collected morphological data, and gave us a better picture of the true taxonomic diversity of parasites and other microorganisms in our host population. Thisresearch was conceptualized and led by me, with lab assistance from Hadjira Hamou, Joelle Hass, and Jessica Churcher, and sample collection by Suheidy Romero Morales and the Sector Santa Rosa Primate Project. In Chapter 4, I explore how group membership and kinship may facilitate the acquisition and transmission of gastrointestinal parasites in wild female capuchin monkeys by surveying a subset of 35 females from all five social groups. Though we were unable to collect corresponding behavioral social data at the time of fecal sample collection due to the COVID-19 pandemic, decades of observing the host population had yielded strong intergenerational kinship and group membership records. I use these previously generated data to examine whether host social factors – such as group identity, group size, the number of female kin in the host’s group, and factors likely affecting patterns of host sociality, such as host age and rank – affected the infection patterns of directly transmitted parasites (Strongyloides and presumably Filariopsis) differently than those of indirectly transmitted parasites, which require an intermediate arthropod host. I also ask if groupmates and kin had more similar patterns of parasitic infection than non- groupmates and non-kin, and if parasitic infections are ‘heritable’. I found that Strongyloides infections in females were more intense and more prevalent in younger individuals, but also more intense in lower ranking individuals. Strongyloides infection intensities had a significant heritable component as did infections with indirectly transmitted parasites. These results suggest that the matrilineal and kin-biased social structure of capuchin monkeys may play a role in shaping their parasitic infections. I conceptualized and conducted all of the analyses for this chapter with a subset of previously collected and screened samples. In Chapter 5, I integrate ranging, climate, and remotely sensed data to further explore what ecological factors might related to seasonal and group-level differences in parasitic infections. Imodel the effects of group size, group home range size, temperature, rainfall, NDVI and landcover on various measures of parasitism and found that population-level factors such as local temperature and rainfall were the only factors that related to patterns of parasitic infection in this host populations. Strongyloides infections were higher in cooler and drier months, while the prevalence of indirectly transmitted parasites was also higher in drier months. These results complement previously conducted research by researchers at the Sector Santa Rosa Primate Project, which found that capuchins show seasonal changes in their diet and behavior that may regulate their exposure to different types of indirectly and environmentally transmitted parasites. In Chapter 6, I summarize the results of this series of studies, explain their limitations, highlight the strengths of conducting parasitological research on long studied and well-known host populations, and provide suggestions for how my findings could be used in future research.
Animal Sciences, Biological and Physical Anthropology, Biology, Ecology and Evolutionary Biology, Genetics, Parasitology, Primatology, Biological Anthropology, Costa Rica
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