Ecology and Epidemiology of Nematode Infection in Japanese Macaques:

MacIntosh, Andrew J. J.

doi:10.2354/psj.30.003

Cited by 8 publications

(7 citation statements)

References 196 publications

(215 reference statements)

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“…However, O. stephanostomum has not been detected in humans living in close proximity to gorillas in Gabon (Makouloutou et al, 2014) or bonobos (Pan paniscus) in the Democratic Republic of the Congo (Narat et al, 2015), Gasser et al (1999) leading some to suggest that strains with differential capacities to infect humans may exist (Ota et al, 2015). O. aculeatum, on the other hand, is the least studied of these nodule worms, with most records of infection coming from macaques in Asia (Japanese macaques [M. fuscata]: Hashimoto & Honjo, 1966, Arizono, Yamada, Tegoshi, & Onishi, 2012, MacIntosh, 2014. Despite the extensive humannonhuman primate interface throughout Asia (Fuentes, 2006), there have been but a few reported human cases in the region, for example, in Indonesia (Siang & Joe, 1953), Brunei (Ross, Gibson, & Harris, 1989), and Malaysia (Karim & Yang, 1992), with little published information regarding the causative agent.…”

Section: Introductionmentioning

confidence: 99%

Molecular characterization of nodule worm in a community of Bornean primates

Frías

Stark

Lynn

et al. 2019

Ecology and Evolution

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Strongyles are commonly reported parasites in studies of primate parasite biodiversity. Among them, nodule worm species are often overlooked as a serious concern despite having been observed to cause serious disease in nonhuman primates and humans. In this study, we investigated whether strongyles found in Bornean primates are the nodule worm Oesophagostomum spp., and to what extent these parasites are shared among members of the community. To test this, we propose two hypotheses that use the parasite genetic structure to infer transmission processes within the community. In the first scenario, the absence of parasite genetic substructuring would reflect high levels of parasite transmission among primate hosts, as primates’ home ranges overlap in the study area. In the second scenario, the presence of parasite substructuring would suggest cryptic diversity within the parasite genus and the existence of phylogenetic barriers to cross‐species transmission. By using molecular markers, we identify strongyles infecting this primate community as O. aculeatum , the only species of nodule worm currently known to infect Asian nonhuman primates. Furthermore, the little to no genetic substructuring supports a scenario with no phylogenetic barriers to transmission and where host movements across the landscape would enable gene flow between host populations. This work shows that the parasite's high adaptability could act as a buffer against local parasite extinctions. Surveys targeting human populations living in close proximity to nonhuman primates could help clarify whether this species of nodule worm presents the zoonotic potential found in the other two species infecting African nonhuman primates.

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Section: Introductionmentioning

confidence: 99%

Molecular characterization of nodule worm in a community of Bornean primates

Frías

Stark

Lynn

et al. 2019

Ecology and Evolution

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“…Rushmore et al [, ] suggested that we might use individual traits that correlate with centrality in disease intervention strategies, based on their results from chimpanzee networks showing that high‐ranking males and individuals with large family units were the most central individuals and thus best to target in vaccination efforts. A related outstanding question is whether or not high dominance rank might allow an individual to better tolerate certain infections [MacIntosh, ], which would make them even more capable of spreading infectious agents [Ezenwa and Jolles, ]. In our study, however, a middle‐ranking old adult female and a low‐ranking adult female exhibited the highest eigenvector centrality coefficients in the Yakushima group, while a middle‐ranking adult female exhibited the highest betweenness coefficient in Koshima group, all by a very wide margin.…”

Section: Discussionmentioning

confidence: 54%

“…In this study, we combine social network analysis of empirical data and agent‐based modeling to investigate the theoretical relationship between network properties and the propagation of infectious agents. We focus on infectious agents transmissible through social contact networks in Japanese macaques, which provide a well studied and thus tractable model system [MacIntosh, ]. Macaques are generally considered the most widely distributed and best studied group of non‐human primates [Thierry, ; Thierry et al, ], and in many parts of their range exist in extreme proximity to human settlements.…”

Section: Introductionmentioning

confidence: 99%

“…Macaques are generally considered the most widely distributed and best studied group of non‐human primates [Thierry, ; Thierry et al, ], and in many parts of their range exist in extreme proximity to human settlements. There is also some empirical evidence that infection by nematode parasites in Japanese macaques specifically is related to network centrality and position within the dominance hierarchy [MacIntosh, ; MacIntosh et al, ]. However, many of the epidemiological processes involved, particularly those concerning other groups of socially transmissible agents in these and other macaque species, remain poorly understood.…”

Section: Introductionmentioning

confidence: 99%

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Modeling infection transmission in primate networks to predict centrality‐based risk

Romano

Duboscq

Sarabian

et al. 2016

American J Primatol

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Social structure can theoretically regulate disease risk by mediating exposure to pathogens via social proximity and contact. Investigating the role of central individuals within a network may help predict infectious agent transmission as well as implement disease control strategies, but little is known about such dynamics in real primate networks. We combined social network analysis and a modeling approach to better understand transmission of a theoretical infectious agent in wild Japanese macaques, highly social animals which form extended but highly differentiated social networks. We collected focal data from adult females living on the islands of Koshima and Yakushima, Japan. Individual identities as well as grooming networks were included in a Markov graph-based simulation. In this model, the probability that an individual will transmit an infectious agent depends on the strength of its relationships with other group members. Similarly, its probability of being infected depends on its relationships with already infected group members. We correlated: (i) the percentage of subjects infected during a latency-constrained epidemic; (ii) the mean latency to complete transmission; (iii) the probability that an individual is infected first among all group members; and (iv) each individual's mean rank in the chain of transmission with different individual network centralities (eigenvector, strength, betweenness). Our results support the hypothesis that more central individuals transmit infections in a shorter amount of time and to more subjects but also become infected more quickly than less central individuals. However, we also observed that the spread of infectious agents on the Yakushima network did not always differ from expectations of spread on random networks. Generalizations about the importance of observed social networks in pathogen flow should thus be made with caution, since individual characteristics in some real world networks appear less relevant than they are in others in predicting disease spread. Am. J. Primatol. 78:767-779, 2016. © 2016 Wiley Periodicals, Inc.

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“…Over the past 11 years, detailed and ongoing studies have been conducted on the prevalence of gastrointestinal parasites in the Ugandan red colobus (e.g., Chapman, Speirs, Gillespie, Holland, & Austad, ; Chapman, Wasserman, et al., ; Gillespie, Chapman, & Greiner, ; Gillespie, Greiner, & Chapman, ). In general, gastrointestinal parasitism is known to influence reproductive fitness by inducing sickness behaviour (Ghai et al., ; Hart, , ), modulating the immune system (MacIntosh, ), and inducing an inflammatory immune response (MacIntosh, ; Marzal, De Lope, Navarro, & Møller, ). For example, disease caused by Trichuris infection is considered a neglected tropical disease that affects an estimated ~800 million people worldwide and is responsible for a variety of clinical symptoms including developmental disabilities, growth stunting and anaemia (Stephenson, Holland, & Cooper, ).…”

Section: Introductionmentioning

confidence: 99%

Cis‐regulatory evolution in a wild primate: Infection‐associated genetic variation drives differential expression of MHC‐DQA1 in vitro

et al. 2017

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Few studies have combined genetic association analyses with functional characterization of infection-associated SNPs in natural populations of non-human 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: 1) MHC-DQA1 regulatory genetic variation is associated with control of whipworm (Trichuris) infection in a natural population of red colobus; 2) infection-associated SNPs are functional in driving differential gene expression in-vitro; and 3) 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 non-coding RADseq data. Our data suggest that balancing selection provides adaptive regulatory flexibility that outweighs the consequences of increased parasite infection intensity in heterozygotes.

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Ecology and Epidemiology of Nematode Infection in Japanese Macaques:

Cited by 8 publications

References 196 publications

Molecular characterization of nodule worm in a community of Bornean primates

Molecular characterization of nodule worm in a community of Bornean primates

Modeling infection transmission in primate networks to predict centrality‐based risk

Cis‐regulatory evolution in a wild primate: Infection‐associated genetic variation drives differential expression of MHC‐DQA1 in vitro

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