Socioecological predictors of immune defences in wild spotted hyenas

Flies, Andrew S.; Mansfield, Linda S.; Flies, Emily J.; Grant, Chris K.; Holekamp, Kay E.

doi:10.1111/1365-2435.12638

Cited by 33 publications

(39 citation statements)

References 70 publications

(121 reference statements)

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“…Some studies did not even report the number of interactions recorded (e.g. Campos & Fedigan, 2013;Flies, Mansfield, Flies, Grant, & Holekamp, 2016;Stewart & Greives, 2016), which hinders the researchers' ability to evaluate the reliability of the results. We suggest that, unless hierarchy is a priori known to be extremely steep (that is, no inconsistencies are found in a large dataset), researchers should aim to record a minimum ratio of interactions to individuals of 10 or ideally 20, to ensure that the dominance hierarchy is reliably inferred.…”

Section: Discussionmentioning

confidence: 99%

A practical guide for inferring reliable dominance hierarchies and estimating their uncertainty

Sánchez‐Tójar

Schroeder

Farine

2017

Journal of Animal Ecology

160

189

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Many animal social structures are organized hierarchically, with some individuals monopolizing resources. Dominance hierarchies have received great attention from behavioural and evolutionary ecologists. There are many methods for inferring hierarchies from social interactions. Yet, there are no clear guidelines about how many observed dominance interactions (i.e. sampling effort) are necessary for inferring reliable dominance hierarchies, nor are there any established tools for quantifying their uncertainty. We simulate interactions (winners and losers) in scenarios of varying steepness (the probability that a dominant defeats a subordinate based on their difference in rank). Using these data, we (1) quantify how the number of interactions recorded and the steepness of the hierarchy affect the performance of five methods for inferring hierarchies, (2) propose an amendment that improves the performance of a popular method, and (3) suggest two easy procedures to measure uncertainty and steepness in the inferred hierarchy. We find that the ratio of interactions to individuals required to infer reliable hierarchies is surprisingly low, but depends on the steepness of the hierarchy and the method used. We show that David's score and our novel randomized Elo-rating are the best methods when hierarchies are not extremely steep, where the original Elo-rating, the I&SI and the recently described ADAGIO perform less well. In addition, we show that two simple methods can be used to estimate uncertainty at the individual and group level, and that the randomized Elo-rating repeatability provides researchers with a standardized measure valid for comparing the steepness of different hierarchies. We provide several worked examples to guide researchers interested in studying dominance hierarchies. Methods for inferring dominance hierarchies are relatively robust. We recommend that a ratio of observed interactions to individuals of at least 10 (for steep hierarchies), and ideally 20 serves as a good benchmark. Our simple procedures for estimating uncertainty in the observed data will facilitate evaluating whether sufficient data have been collected, while plotting the shape of the hierarchy will provide new insights into the social structure of the study organism.

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Section: Discussionmentioning

confidence: 99%

A practical guide for inferring reliable dominance hierarchies and estimating their uncertainty

Sánchez‐Tójar

Schroeder

Farine

2017

Journal of Animal Ecology

160

189

View full text Add to dashboard Cite

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“…Similarly, nutritionally disadvantaged hyenas suffered higher mortality during an outbreak of a pathogenic bacterium (Höner et al., ). Higher serum concentrations of the immunoglobulin IgM in high‐ranking females may reflect a greater allocation of resources to immune processes (Flies et al., ). Rank‐related differences in the expression of immune genes have been reported in a non‐human primate (Tung et al., ).…”

Section: Discussionmentioning

confidence: 99%

“…On the other hand, there is strong evidence that a high social position within the sex‐specific linear dominance hierarchies has major benefits for hyenas in terms of their access to resources and fitness (Hofer & East, ; Holekamp, Smale, & Szykman, ; Höner et al., ), allostatic load (“stress”) (Goymann et al., ) and allocation of resources to immune processes (East et al., ; Flies, Mansfield, Flies, Grant, & Holekamp, ). Thus, the allocation hypothesis predicts that high‐ranking hyenas are less likely to get infected with CDV and more likely to survive the infection than low‐ranking hyenas (Figure ).…”

Section: Introductionmentioning

confidence: 99%

Social status mediates the fitness costs of infection with canine distemper virus in Serengeti spotted hyenas

et al. 2018

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The extent to which the fitness costs of infection are mediated by key life‐history traits such as age or social status is still unclear. Within populations, individual heterogeneity in the outcome of infection is the result of two successive processes; the degree of contact with the pathogen (exposure) and the immune response to infection. In social mammals, because individuals holding high social status typically interact more frequently with group members, they should be more often in contact with infected individuals than those of low social status. However, when access to resources is determined by social status, individuals with a high social status are often better nourished, have a greater opportunity to allocate resources to immune processes and therefore should have a smaller chance of succumbing to infection than individuals with low social status. We investigated the risk and fitness costs of infection during a virulent epidemic of canine distemper virus (CDV) in a social carnivore, the spotted hyena, in the Serengeti National Park. We analysed two decades of detailed life‐history data from 625 females and 816 males using a multi‐event capture–mark–recapture model that accounts for uncertainty in the assignment of individual infection states. Cubs of mothers with a high social status had a lower probability of CDV infection and were more likely to survive infection than those with low social status. Subadult and adult females with high social status had a higher infection probability than those with low social status. Subadult females and pre‐breeder males that had recovered from CDV infection had a lower survival than susceptible ones. Our study disentangles the relative importance of individual exposure and resource allocation to immune processes, demonstrates fitness costs of infection for juveniles, particularly for those with low social status, shows that patterns of infection can be driven by different mechanisms among juveniles and adults and establishes a negative relationship between infection and fitness in a free‐ranging mammal. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13059/suppinfo is available for this article.

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“…Thus, high-ranking juveniles are expected to exhibit greater tolerance of infection than low-ranking juveniles. Several studies provide evidence that adult high-ranking individuals do allocate more resources to immune processes and the repair of parasite damaged tissue than low-ranking animals (Ardia et al, 2011;East et al, 2015;Flies, Mansfield, Flies, Grant, & Holekamp, 2016;Marescot et al, 2018), but studies of this kind on juveniles are rare.…”

Section: Introductionmentioning

confidence: 99%

Parasite infections in a social carnivore: Evidence of their fitness consequences and factors modulating infection load

Ferreira

Hofer

Carvalho

et al. 2019

Ecology and Evolution

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There are substantial individual differences in parasite composition and infection load in wildlife populations. Few studies have investigated the factors shaping this heterogeneity in large wild mammals or the impact of parasite infections on Darwinian fitness, particularly in juveniles. A host's parasite composition and infection load can be shaped by factors that determine contact with infective parasite stages and those that determine the host's resistance to infection, such as abiotic and social environmental factors, and age. Host–parasite interactions and synergies between coinfecting parasites may also be important. We test predictions derived from these different processes to investigate factors shaping infection loads (fecal egg/oocyte load) of two energetically costly gastrointestinal parasites: the hookworm Ancylostoma and the intracellular Cystoisospora , in juvenile spotted hyenas ( Crocuta crocuta ) in the Serengeti National Park, in Tanzania. We also assess whether parasite infections curtail survival to adulthood and longevity. Ancylostoma and Cystoisospora infection loads declined as the number of adult clan members increased, a result consistent with an encounter‐reduction effect whereby adults reduced encounters between juveniles and infective larvae, but were not affected by the number of juveniles in a clan. Infection loads decreased with age, possibly because active immune responses to infection improved with age. Differences in parasite load between clans possibly indicate variation in abiotic environmental factors between clan den sites. The survival of juveniles (<365 days old) to adulthood decreased with Ancylostoma load, increased with age, and was modulated by maternal social status. High‐ranking individuals with low Ancylostoma loads had a higher survivorship during the first 4 years of life than high‐ranking individuals with high Ancylostoma loads. These findings suggest that high infection loads with energetically costly parasites such as hookworms during early life can have negative fitness consequences.

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Socioecological predictors of immune defences in wild spotted hyenas

Cited by 33 publications

References 70 publications

A practical guide for inferring reliable dominance hierarchies and estimating their uncertainty

A practical guide for inferring reliable dominance hierarchies and estimating their uncertainty

Social status mediates the fitness costs of infection with canine distemper virus in Serengeti spotted hyenas

Parasite infections in a social carnivore: Evidence of their fitness consequences and factors modulating infection load

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