Parasitism and host social behaviour: a meta-analysis of insights derived from social network analysis

Briard, Léa; Ezenwa, Vanessa O.

doi:10.1016/j.anbehav.2020.11.010

Cited by 24 publications

(44 citation statements)

References 48 publications

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“…As in our study, not all network metrics could predict infection intensity, but both investigations now suggest that eigenvector centrality, whether in grooming or in proximity networks, is associated with nematode parasitism in Japanese macaques. Our results also align with a recent meta-analysis of studies investigating parasites in host social networks, wherein strength and eigenvector centrality showed stronger associations with parasitism than did any of betweenness, closeness or degree centrality (Briard and Ezenwa, 2021). It therefore seems important to consider what these various centrality measures represent in terms of host socio-biology, and in terms of social or ecological processes.…”

Section: Discussionsupporting

confidence: 91%

“…It therefore seems important to consider what these various centrality measures represent in terms of host socio-biology and in terms of social or ecological processes. Exposure and transmission risk of fast and directly spread parasites such as lice or certain viruses and bacteria might depend simply on the number of associations individuals have (degree), whereas slower-spreading/developing parasites or those requiring additional developmental stages in the environment may be more dependent on the actual time hosts spend in contact or in spatial proximity with one another (strength), or the overall degree of social integration they have (eigenvector centrality) (Silk et al, 2017; Briard and Ezenwa, 2021; Lucatelli et al, 2021). By whatever mechanism, our results support those of review studies and meta-analyses showing that, across many different sociality measures and parasites with different life histories and modes of transmission, the relationship between sociality and parasitism is generally positive (Altizer et al, 2003; Rushmore et al, 2017; Briard and Ezenwa, 2021; Lucatelli et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

“…In cases such as the latter, carefully designed experiments are required to test the mechanisms linking networks to infection. But in general, such links have been demonstrated in a broad array of contexts, regardless of the type of network or parasite species under study, or even the measures of parasitism used (Altizer et al, 2003; Ezenwa et al, 2016; Rushmore et al, 2017; Briard and Ezenwa, 2021; Lucatelli et al, 2021).…”

Section: Introductionmentioning

confidence: 99%

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

Wang

MacIntosh

Castellano-Navarro

et al. 2021

Preprint

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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 is often associated with increased parasite abundance or diversity. The social structure of a group or population has been shown to be paramount to patterns of infection and transmission. Yet, for various reasons, studies investigating the social transmission of parasites in animals, and especially in primates, have only taken into account parts of the group (e.g., only adults or even only adult females), which is likely to impact the interpretation of any results linking sociality and parasitism. Here, we investigated the relationship between social network centrality and an estimate of gastrointestinal helminth infection intensity in a complete group of Japanese macaques (Macaca fuscata). We then tested the impact of missing parts of the group on this relationship. We aimed to test: (1) whether social network centrality - the number of partners (degree), frequency of interactions (strength) and level of social integration (eigenvector) - was linked to parasite infection intensity; and, (2) to what extent excluding all or portions of individuals within the group from the analyses might influence the observed relationship. We conducted social network analysis on data collected from one complete group of Japanese macaques over two months on Koshima Island, Japan, to relate metrics of network centrality to an index of parasite infection intensity (eggs per gram of feces: EPG). We then ran a series of knock-out simulations to test the effect(s) of accounting only for certain age-sex classes on the observed relationship. General linear mixed models showed that, in the complete network, centrality was positively associated with infection by the examined geohelminths (Oesophagostomum aculeatum, Trichuris trichiura and Strongyloides fuelleborni), but in partial networks with only adult females, only juveniles, or random subsets of the group, the strength of this relationship - albeit still positive - lost statistical significance. Our study indicates that sampling bias can impact the relationship that is observed between social interaction and parasitism. In addition to supporting earlier results linking geohelminths to Japanese macaque social networks, this work introduces important methodological considerations for research into the dynamics of social transmission, with applications to infectious disease epidemiology, population management, and health interventions.

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Section: Discussionsupporting

confidence: 91%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Wang

MacIntosh

Castellano-Navarro

et al. 2021

Preprint

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“…Predators drive defensive group-living in animals across taxa 6 , which can increase parasitism 48 , creating ecological and evolutionary feedbacks between host sociality and parasites 47 . Parasites evolve along virulence-transmission trade-offs in systems ranging from viruses of humans 16 , bacterial pathogens of birds 14 , protozoan pathogens of insects 15 , and our monogenean fish ectoparasite.…”

Section: Eco-coevolutionary Model Resolves Complexity To Show That Social Hosts Have Deadlier Parasitesmentioning

confidence: 99%

Social hosts evade predation but have deadlier parasites

Walsman

Janecka

Clark

et al. 2021

Preprint

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Parasites exploit hosts to replicate and transmit, but overexploitation kills both host and parasite: parasite virulence evolves to balance these costs and benefits. Predators can in theory shift this balance by consuming hosts. However, the non-consumptive effects of predators may be as important as their consumptive effects. Here, we use an eco-coevolutionary model to show that predators select for host grouping, a common anti-predator, defensive social behaviour. Host grouping simultaneously increases parasite transmission, thus within-host parasite competition, and therefore favours more exploitative, virulent, parasites. When parametrized with data from the guppy-Gyrodactylus spp. system, including our experimentally demonstrated trade-off between virulence and transmission, our model accurately predicted the common garden-assayed virulence of 18 parasite lines collected from four Trinidadian guppy populations under different predation regimes. The quantitative match between theory and data lends credence to the model insight that the non-consumptive, social behaviour pathway is entirely responsible for the observed increase in virulence with predation pressure. Our results indicate that parasites play an important, underappreciated role in guppy evolutionary ecology. Moreover, group living is a common anti-predator defence and our general model accommodates host-parasite interactions across taxa: its insight into the interactions among predation, sociality, and virulence evolution may apply broadly. Our results additionally suggest that social distancing, by reducing host-host contact, can select for less virulent parasites and pathogens.

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“…While our focus here was solely on time spent grooming, social interaction has been linked to infection susceptibility and transmission in several social species [53][54][55] including non-human primates [56,57]. This suggests that, despite the lack of change in the time spent grooming, increased parasite load may result in alternative suppressive strategies, such as changes in the number or identity of grooming partners.…”

Section: Discussionmentioning

confidence: 99%

Sick and Tired: Polyparasitism, Food Stress and Sickness Behaviour in a Gregarious Mammal

Blersch

Ganswindt

et al. 2021

Preprint

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Although sickness behaviour in response to non-lethal parasites has been documented in wild animals, it remains unclear how social and environmental stress might also shape an animal's behavioural response to parasitism, nor do we know whether simultaneous infection with more than one parasite changes the way animals respond. Here, we combine physiological, environmental, behavioural and parasite measures to investigate behavioural responses to infection in wild vervet monkeys (Chlorocebus pygerythrus) living in a semi-arid region of South Africa. We quantified both activity budget and behavioural predictability to investigate the occurrence of sickness behaviour and infection with two non-lethal gastrointestinal parasite genera. Higher parasite load was linked to an increase in the time spent resting. However, the nature of the relationship with other behaviours was contingent on both the parasite genus in question, and how parasite species interacted, highlighting the importance of considering co-infection. Overall, food availability was the dominant predictor of behavioural change suggesting that, for monkeys living in a more extreme environment, coping with ecological stress may override the ability to modulate behaviour in response to other physiological stressors. Our findings provide insight into how animals living in harsh environments find ways to cope with parasite infection, avoidance, and transmission.

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Parasitism and host social behaviour: a meta-analysis of insights derived from social network analysis

Cited by 24 publications

References 48 publications

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

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

Social hosts evade predation but have deadlier parasites

Sick and Tired: Polyparasitism, Food Stress and Sickness Behaviour in a Gregarious Mammal

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