Linking parasitism to network centrality and the impact of sampling bias in its interpretation

Group living is beneficial for individuals, but also comes with costs. One such cost is the increased possibility of pathogen transmission because increased numbers or frequencies of social contacts are often associated with increased parasite abundance or diversity. The social structure of a group or population is paramount to patterns of infection and transmission. Yet, for various reasons, studies investigating the links between sociality and parasitism in animals, especially in primates, have only accounted for parts of the group (e.g., only adults), which is likely to impact the interpretation of results. Here, we investigated the relationship between social network centrality and an estimate of gastrointestinal helminth infection intensity in a whole group of Japanese macaques (Macaca fuscata). We then tested the impact of omitting parts of the group on this relationship. We aimed to test: (1) whether social network centrality –in terms of the number of partners (degree), frequency of interactions (strength), and level of social integration (eigenvector) –was linked to parasite infection intensity (estimated by eggs per gram of faeces, EPG); and, (2) to what extent excluding portions of individuals within the group might influence the observed relationship. We conducted social network analysis on data collected from one group of Japanese macaques over three months on Koshima Island, Japan. We then ran a series of knock-out simulations. General linear mixed models showed that, at the whole-group level, network centrality was positively associated with geohelminth infection intensity. However, in partial networks with only adult females, only juveniles, or random subsets of the group, the strength of this relationship - albeit still generally positive - lost statistical significance. Furthermore, knock-out simulations where individuals were removed but network metrics were retained from the original whole-group network showed that these changes are partly a power issue and partly an effect of sampling the incomplete network. Our study indicates that sampling bias can thus hamper our ability to detect real network effects involving social interaction and parasitism. In addition to supporting earlier results linking geohelminth infection to Japanese macaque social networks, this work introduces important methodological considerations for research into the dynamics of social transmission, with implications for infectious disease epidemiology, population management, and health interventions

Lurking in the dark: cryptic Strongyloides in a Bornean slow loris

Within host communities, related species are more likely to share common parasitic agents, and as a result, morphological similarities have led researchers to conclude that parasites infecting closely related hosts within a community represent a single species. However, genetic diversity within parasite genera and host range remain poorly investigated in most systems. Strongyloides is a genus of soil-transmitted nematode that has been reported from several primate species in Africa and Asia, and has been estimated to infect hundreds of millions of people worldwide, although no precise estimates are available. Here we describe a case of infection with a cryptic species of Strongyloides in a Bornean (Philippine) slow loris (Nycticebus menagensis) living within a diverse community of several primate species in the Lower Kinabatangan Wildlife Sanctuary, Malaysian Borneo. Fresh fecal samples were collected from five primate species and nematode larvae cultured from these samples were selected for phylogenetic analyses. Sequences obtained for most larvae were identified as S. fuelleborni, grouping into three different clusters and showing no aggregation within specific hosts or geographic location. In contrast, a set of parasite sequences obtained from a slow loris clustered closely with S. stercoralis into a different group, being genetically distinct to sequences reported from other primate hosts, humans included. Our results suggest that although S. fuelleborni infects all haplorrhines sampled in this primate community, a different species might be infecting the slow loris, the only strepsirrhine in Borneo and one of the least studied primates in the region. Although more data are needed to support this conclusion, we propose that Strongyloides species in primates might be more diverse than previously thought, with potential implications for ecological and evolutionary host-parasite associations, as well as epidemiological dynamics

A pinworm's tale: The evolutionary history of Lemuricola (Protenterobius) nycticebi

Lemuricola (Protenterobius) nycticebi is the only pinworm species known to infect strepsirrhine primates outside Africa, and the only pinworm species yet described in slow lorises. Here, we provided a detailed morphological comparison of female and male worms, and a first description of fourth-stage larvae collected from free-living slow lorises (Nycticebus menagensis) in Sabah, Malaysian Borneo. Using mitochondrial and nuclear markers, we also reconstructed the species' phylogenetic relationship with other pinworms infecting primates. Both morphological and molecular results indicated a distinct association between L. (P.) nycticebi and its host. However, while taxonomy identified this species as a member of the Lemuricola clade and grouped pinworms infecting lemurs and slow lorises together, phylogenetic reconstruction split them, placing L. (P.) nycticebi within the Enterobius clade. Our results suggest that L. (P.) nycticebi may represent a different taxon altogether, and that it is more closely related to pinworm species infecting Old World primates outside Madagascar. Pongobius pongoi (Foitová et al., 2008) n. comb. is also proposed

Parasite community structure in sympatric Bornean primates

Parasites are important components of ecosystems, influencing trophic networks, competitive interactions and biodiversity patterns. Nonetheless, we are not nearly close to disentangling their complex roles in natural systems. Southeast Asia falls within global areas targeted as most likely to source parasites with zoonotic potential, where high rates of land conversion and fragmentation have altered the circulation of wildlife species and their parasites, potentially resulting in altered host-parasite systems. Although the overall biodiversity in the region predicts equally high, or even higher, parasite diversity, we know surprisingly little about wild primate parasites, even though this constitutes the first step towards a more comprehensive understanding of parasite transmission processes. Here, we characterise the gastrointestinal helminth parasite assemblages of a community of Bornean primates living along the Kinabatangan floodplain in Sabah (Malaysian Borneo), including two species endemic to the island. Through parasitological analyses, and by using several measures of parasite infection as proxies for parasite diversity and distribution, we show that (i) most parasite taxonomic groups are not limited to a single host, suggesting a greater flexibility for habitat disturbance, (ii) parasite infracommunities of nocturnal primates differ from their diurnal counterparts, reflecting both phylogenetic and ecological constraints, and (iii) soil-transmitted helminths such as whipworm, threadworm and nodule worm are widespread across the primate community. This study also provides new parasite records for southern pig-tailed macaques (Macaca nemestrina), silvered langurs (Trachypithecus cristatus) and Western tarsiers (Cephalopachus bancanus) in the wild, while adding to the limited records for the other primate species in the community. Given the information gap regarding primate-parasite associations in the region, the information presented here should prove relevant for future studies of parasite biodiversity and infectious disease ecology in Asia and elsewhere

Novel insight into the genetic diversity of strongylid nematodes infecting South-East and East Asian primates

With many non-human primates (NHPs) showing continued population decline, there is an ongoing need to better understand their ecology and conservation threats. One such threat is the risk of disease, with various bacterial, viral and parasitic infections previously reported to have damaging consequences for NHP hosts. Strongylid nematodes are one of the most commonly reported parasitic infections in NHPs. Current knowledge of NHP strongylid infections is restricted by their typical occurrence as mixed infections of multiple genera, which are indistinguishable through traditional microscopic approaches. Here, modern metagenomics approaches were applied for insight into the genetic diversity of strongylid infections in South-East and East Asian NHPs. We hypothesized that strongylid nematodes occur in mixed communities of multiple taxa, dominated by Oesophagostomum, matching previous findings using single-specimen genetics. Utilizing the Illumina MiSeq platform, ITS-2 strongylid metabarcoding was applied to 90 samples from various wild NHPs occurring in Malaysian Borneo and Japan. A clear dominance of Oesophagostomum aculeatum was found, with almost all sequences assigned to this species. This study suggests that strongylid communities of Asian NHPs may be less species-rich than those in African NHPs, where multi-genera communities are reported. Such knowledge contributes baseline data, assisting with ongoing monitoring of health threats to NHPs

The tradeoff between information and pathogen transmission in animal societies

Social structure can regulate information and pathogen transmission via social contact or proximity, which ultimately affects individual fitness. In theory, the same network properties that favor social information transmission also favor the spread of socially-transmitted pathogens, creating a trade-off between them. The mechanisms underlying the development and stability of individual relationships considering this trade-off remain underexplored. Here, we outline the evolutionary mechanisms of social transmission and hypothesize that network topology can be optimized in a way that balances the costs and benefits of social relationships. In this context, emergent network properties might reflect a trade-off between information and pathogen transmission in animal societies. We then propose an implementation of Hinde’s classical framework by incorporating the costs of socializing in a negative feedback loop in the emergence of social structure. We hope this manuscript encourages research into this underxplored social trade-off and the evolutionary processes underlying it

Stemming the Flow: Information, Infection, and Social Evolution

International audienceSocial information and socially transmitted pathogens are governed by social structure, and also shape social interactions. However, information and infection are rarely investigated as interactive factors driving social evolution. We propose exactly such an integrative framework, drawing attention to mechanisms of social phenotypic plasticity for information spread and pathogen control

Network centrality and seasonality interact to predict lice load in a social primate

International audienceLice are socially-transmitted ectoparasites. Transmission depends upon their host’s degree of contactwith conspecifics. While grooming facilitates ectoparasite transmission via body contact, it alsoconstrains their spread through parasite removal. We investigated relations between parasite burdenand sociality in female Japanese macaques following two opposing predictions: i) central females incontact/grooming networks harbour more lice, related to their numerous contacts; ii) central femalesharbour fewer lice, related to receiving more grooming. We estimated lice load non-invasively usingthe conspicuous louse egg-picking behaviour performed by macaques during grooming. We tested forcovariation in several centrality measures and lice load, controlling for season, female reproductivestate and dominance rank. Results show that the interaction between degree centrality (number ofpartners) and seasonality predicted lice load: females interacting with more partners had fewer licethan those interacting with fewer partners in winter and summer, whereas there was no relationshipbetween lice load and centrality in spring and fall. This is counter to the prediction that increasedcontact leads to greater louse burden but fits the prediction that social grooming limits louse burden.Interactions between environmental seasonality and both parasite and host biology appeared tomediate the role of social processes in louse burden

Faecal avoidance differs between the sexes but not with nematode infection risk in mandrills

International audienceAnimals have evolved a wide range of behaviours that act as barriers to decrease the risk of parasite infection. Faecal avoidance may, for example, limit contact with orofaecally transmitted parasites, such as gastrointestinal nematodes. When present in faeces, however, nematode eggs need to mature before reaching their infective stage. If strategies have evolved in hosts to specifically avoid nematodes, old faeces with infective larvae should elicit stronger avoidance behaviour than fresh faeces that contain noninfective stages. Here, we carried out two experiments to test the hypothesis that mandrills, Mandrillus sphinx, an Old-World primate, exhibit specific behavioural strategies to avoid nematode infection. Our results show that individuals did not avoid faeces in a nonfeeding context but did avoid eating food items contaminated with faecal material, females more so than males. However, neither the presence of nematodes nor the age of faeces influenced the level of avoidance observed, suggesting that mandrills avoid faecal material in general rather than nematodes specifically when foraging

Fractal measures in activity patterns: Do gastrointestinal parasites affect the complexity of sheep behaviour?

International audienceGastrointestinal nematodes are known to be one of the most economically important parasites in livestock production. In order to test whether fractal analysis of behaviour can be used as a diagnostic tool for detection of infected animals, we investigated fractal patterns in the behavioural activity of domestic sheep (Ovis aries) in relation to strongylid infection. Temporal dynamics in activity patterns of 20 sheep were recorded at high resolutions using tri-axial accelerometer loggers attached to the neck of naturally infected subjects. We measured fractal dynamics in the resultant acceleration time series, divided into periods of activity and inactivity, using several fractal methods and tested the prediction that temporal complexity in the activity patterns of infected control sheep and experimentally dewormed sheep should differ. Detrended fluctuation analysis (DFA) revealed that sheep behaviour sequences were characterized by long-range correlations, meaning that acceleration fluctuations are not random but depend on long-term activity events. Generalized linear mixed models built to test for the effect of deworming on fractal estimates showed that the temporal organization of sheep activity varies with the status of strongylid infection. Our results indicate that sheep treated with anthelmintics exhibited a higher complexity in their activity sequences than parasitized sheep, suggesting that organizational patterns of their behaviour change with gastrointestinal parasite infection. Thus, we provide evidence for the potential utility of fractal methods in behavioural welfare monitoring