Ecology eclipses phylogeny as a major driver of nematode parasite community structure in a graminivorous primate

Understanding how ecology and phylogeny shape parasite communities can inform parasite control and wildlife conservation initiatives while contributing to the study of host species evolution.We tested the relative strengths of phylogeny and ecology in driving parasite community structure in a host whose ecology diverges significantly from that of its closest phylogenetic relatives.We characterized the gastrointestinal (GI) parasite community of wild geladas Theropithecus gelada, primates that are closely related to baboons but specialized to graminovory in the Ethiopian Highlands.Geladas exhibited very constrained GI parasite communities: only two genera (Oesophagostomum and Trichostrongylus) were identified across 305 samples. This is far below the diversity reported for baboons (Papio spp.) and at the low end of the range of domestic grazers (e.g. Bos taurus, Ovis aries) inhabiting the same region and ecological niche.Using deep amplicon sequencing, we identified 15 amplicon sequence variants (ASVs) within the two genera, seven of which matched to Oesophagostomum sp., seven to Trichostrongylus sp., and one to T. vitrinus.Population was an important predictor of ASV richness. Geladas in the most ecologically disturbed area of the national park exhibited approximately four times higher ASV richness than geladas at a less disturbed location within the park.In this system, ecology was a stronger predictor of parasite community structure than was phylogeny, with geladas sharing more elements of their parasite communities with other grazers in the same area than with closely related sister taxa.A free Plain Language Summary can be found within the Supporting Information of this article.A free Plain Language Summary can be found within the Supporting Information of this article.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/162742/3/fec13603_am.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162742/2/fec13603.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162742/1/fec13603-sup-0001-Summary.pd

Identifying wildlife reservoirs of neglected taeniid tapeworms : non-invasive diagnosis of endemic Taenia serialis infection in a wild primate population

Despite the global distribution and public health consequences of Taenia tapeworms, the life cycles of taeniids infecting wildlife hosts remain largely undescribed. The larval stage of Taenia serialis commonly parasitizes rodents and lagomorphs, but has been reported in a wide range of hosts that includes geladas (Theropithecus gelada), primates endemic to Ethiopia. Geladas exhibit protuberant larval cysts indicative of advanced T. serialis infection that are associated with high mortality. However, non-protuberant larvae can develop in deep tissue or the abdominal cavity, leading to underestimates of prevalence based solely on observable cysts. We adapted a non-invasive monoclonal antibody-based enzyme-linked immunosorbent assay (ELISA) to detect circulating Taenia spp. antigen in dried gelada urine. Analysis revealed that this assay was highly accurate in detecting Taenia antigen, with 98.4% specificity, 98.5% sensitivity, and an area under the curve of 0.99. We used this assay to investigate the prevalence of T. serialis infection in a wild gelada population, finding that infection is substantially more widespread than the occurrence of visible T. serialis cysts (16.4% tested positive at least once, while only 6% of the same population exhibited cysts). We examined whether age or sex predicted T. serialis infection as indicated by external cysts and antigen presence. Contrary to the female-bias observed in many Taenia-host systems, we found no significant sex bias in either cyst presence or antigen presence. Age, on the other hand, predicted cyst presence (older individuals were more likely to show cysts) but not antigen presence. We interpret this finding to indicate that T. serialis may infect individuals early in life but only result in visible disease later in life. This is the first application of an antigen ELISA to the study of larval Taenia infection in wildlife, opening the doors to the identification and description of infection dynamics in reservoir populations

Ecology eclipses phylogeny as a major driver of nematode parasite community structure in a graminivorous primate

Understanding how ecology and phylogeny shape parasite communities can inform parasite control and wildlife conservation initiatives while contributing to the study of host species evolution.We tested the relative strengths of phylogeny and ecology in driving parasite community structure in a host whose ecology diverges significantly from that of its closest phylogenetic relatives.We characterized the gastrointestinal (GI) parasite community of wild geladas Theropithecus gelada, primates that are closely related to baboons but specialized to graminovory in the Ethiopian Highlands.Geladas exhibited very constrained GI parasite communities: only two genera (Oesophagostomum and Trichostrongylus) were identified across 305 samples. This is far below the diversity reported for baboons (Papio spp.) and at the low end of the range of domestic grazers (e.g. Bos taurus, Ovis aries) inhabiting the same region and ecological niche.Using deep amplicon sequencing, we identified 15 amplicon sequence variants (ASVs) within the two genera, seven of which matched to Oesophagostomum sp., seven to Trichostrongylus sp., and one to T. vitrinus.Population was an important predictor of ASV richness. Geladas in the most ecologically disturbed area of the national park exhibited approximately four times higher ASV richness than geladas at a less disturbed location within the park.In this system, ecology was a stronger predictor of parasite community structure than was phylogeny, with geladas sharing more elements of their parasite communities with other grazers in the same area than with closely related sister taxa.A free Plain Language Summary can be found within the Supporting Information of this article.A free Plain Language Summary can be found within the Supporting Information of this article.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/162742/3/fec13603_am.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162742/2/fec13603.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162742/1/fec13603-sup-0001-Summary.pd

Urinary neopterin reflects immunological variation associated with age, helminth parasitism, and the microbiome in a wild primate

AbstractNeopterin, a product of activated white blood cells, is a marker of nonspecific inflammation that can capture variation in immune investment or disease-related immune activity and can be collected noninvasively in urine. Mounting studies in wildlife point to lifetime patterns in neopterin related to immune development, aging, and certain diseases, but rarely are studies able to assess whether neopterin can capture multiple concurrent dimensions of health and disease in a single system. We assessed the relationship between urinary neopterin stored on filter paper and multiple metrics of health and disease in wild geladas (Theropithecus gelada), primates endemic to the Ethiopian highlands. We tested whether neopterin captures age-related variation in inflammation arising from developing immunity in infancy and chronic inflammation in old age, inflammation related to intramuscular tapeworm infection, helminth-induced anti-inflammatory immunomodulation, and perturbations in the gastrointestinal microbiome. We found that neopterin had a U-shaped relationship with age, no association with larval tapeworm infection, a negative relationship with metrics related to gastrointestinal helminth infection, and a negative relationship with microbial diversity. Together with growing research on neopterin and specific diseases, our results demonstrate that urinary neopterin can be a powerful tool for assessing multiple dimensions of health and disease in wildlife.</jats:p

Counts of log sample index values (IVs) (the optical density of each sample indexed to the positive and negative controls on each plate) + a constant.

<p>Blue bars indicate samples from individuals without cysts, while grey bars indicate samples from individuals with cysts. The dotted line indicates the optimal threshold cutoff for positive samples indicating antigen presence calculated with the ROC analysis.</p

AICc model selection for predictors of <i>T</i>. <i>serialis</i> antigen-positivity in gelada urine.

<p>AICc model selection for predictors of <i>T</i>. <i>serialis</i> antigen-positivity in gelada urine.</p

Full model averaged coefficient estimates for the predictors of <i>T</i>. <i>serialis</i> cysts in geladas (Model 1), and the predictors of antigen-positivity (Models 2 & 3).

<p>Full model averaged coefficient estimates for the predictors of <i>T</i>. <i>serialis</i> cysts in geladas (Model 1), and the predictors of antigen-positivity (Models 2 & 3).</p

Ag-ELISA results of gelada samples (true positive, true negative, unknown status).

<p>Ag-ELISA results of gelada samples (true positive, true negative, unknown status).</p

Receiver operator characteristic (ROC) curve of antigen ELISA detection of <i>T</i>. <i>serialis</i> infection in dried gelada urine.

<p>The optimal threshold cutoff index value (42.1) had an estimated specificity of 98.4% (95% CI: 95.1–1) and an estimated sensitivity of 98.5% (95% CI: 95.6–1).</p

Identifying wildlife reservoirs of neglected taeniid tapeworms: Non-invasive diagnosis of endemic <i>Taenia serialis</i> infection in a wild primate population - Fig 1

<p>(A) Gelada with a cyst characteristic of confirmed larval <i>T</i>. <i>serialis</i> infections protruding from the abdomen. (B) Internal view of coenuri in the cyst of an infected individual necropsied upon natural death.</p