Does lactation lead to resource allocation trade-offs in the spotted hyaena?

East, Marion L.; Otto, Ellen; Helms, Janine; Thierer, Dagmar; Cable, Joanne; Hofer, Heribert

doi:10.1007/s00265-015-1897-x

Cited by 44 publications

(57 citation statements)

References 76 publications

(99 reference statements)

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“…Our analyses revealed that changes in FEC across the season were influenced by reproductive effort: females that reproduced (Figure , Supporting Information Table S1) and those that produced heavier litters (Figure b, Supporting Information Table S2) exhibited steeper rises in FEC across the season. These observations mirror the reproduction‐induced increase in parasite burden exhibited in many studies previously, including in Soays (Leivesley et al, ), bighorn sheep Ovis canadensis (Festa‐Bianchet, ), domestic sheep (Beasley et al, ) and other wild vertebrates (East et al, ; Knowles et al, ; Nordling et al, ). These results could potentially be attributed to two mechanisms: a cost of reproduction, in the form of fewer resources remaining for allocation to immune‐mediated parasite resistance (Sheldon & Verhulst, ), or an increase in exposure across the season as hungry females spend more time foraging in nutrient‐rich, but also parasite‐rich tussock vegetation (Hutchings, Milner, Gordon, Kyriazakis, & Jackson, ).…”

Section: Discussionsupporting

confidence: 80%

Reproductive effort influences intra‐seasonal variation in parasite‐specific antibody responses in wild Soay sheep

Hayward

Pilkington²,

Wilson

et al. 2019

Functional Ecology

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A trade‐off between reproduction and immune function has been suggested to potentially underpin between‐individual and genetic variation in reproductive strategy, immunity and life span, with potential consequences for host and parasite dynamics. Previous studies in wild animal populations have shown that experimentally induced or natural variation in reproductive effort is negatively associated with general immune markers. Few studies, however, have tackled this question by measuring specific immune responses against prevalent pathogens, and only rarely has variation in immune measures been linked to parasite burden, making it impossible to draw conclusions about the functional relevance of covariation between reproductive effort and immune markers. We collected faecal samples in a longitudinal manner from wild female Soay sheep across late pregnancy and early lactation and measured gastrointestinal nematode faecal egg count (FEC) and worm‐specific antibody responses. Faecal egg count was highly repeatable, with c. 80% of variation due to between‐individual differences, while three isotypes of worm‐specific and total antibodies had moderate repeatability (range: 11%–43%). Females making a greater reproductive effort (those that reproduced, and especially those with heavier litters) showed a more rapid increase in FEC across the season, while non‐reproducing females and those producing lighter litters experienced lower FEC and had higher antibody levels. Associations between antibodies and FEC were complex: worm‐specific immunoglobulin (Ig) G was negatively associated with FEC, while total IgM was positively associated, emphasizing the importance of measuring both immune markers and parasite burden in ecological studies. Our results support the predicted trade‐off between reproductive effort and parasite‐specific immunity: high reproductive effort can limit the ability of individuals to defend themselves against prevalent parasites, with potential downstream consequences for fitness and parasite transmission. A plain language summary is available for this article.

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Section: Discussionsupporting

confidence: 80%

Reproductive effort influences intra‐seasonal variation in parasite‐specific antibody responses in wild Soay sheep

Hayward

Pilkington²,

Wilson

et al. 2019

Functional Ecology

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“…We continuously monitored three hyena clans located at the centre of the Serengeti NP (East et al., ; Hofer & East, ) between 1990 and 2010. Data were collected from all clan members and individuals were identified by their unique spot patterns, scars and other characteristics such as ear notches.…”

Section: Methodsmentioning

confidence: 99%

“…There may be substantial variation among members of a group in their degree of exposure to a given pathogen and in the outcome of infection (Beldomenico & Begon, ; VanderWaal & Ezenwa, ). Body condition and the ability to allocate resources to immune processes can profoundly affect the outcome of infection as can sex, age and social status (East et al., ; Schmid‐Hempel, ). Quantifying individual differences in the outcome of infection and determining the impact of infection on Darwinian fitness in wildlife populations may be a challenge because diagnosing the infection status for large numbers of individuals is difficult in practice, particularly if only non‐invasive methods are available (Gimenez, Lebreton, Gaillard, Choquet, & Pradel, ; McClintock et al., ).…”

Section: Introductionmentioning

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%

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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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“…We also compared these results with those generated by the classical coprological method of parasite egg or oocyst counts as applied, for instance, by East et al (2015) to assess whether the results of these methods were strongly correlated.…”

Section: Introductionmentioning

confidence: 99%

The Intestinal Eukaryotic and Bacterial Biome of Spotted Hyenas: The Impact of Social Status and Age on Diversity and Composition

Heitlinger

Ferreira

Thierer

et al. 2017

Front. Cell. Infect. Microbiol.

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In mammals, two factors likely to affect the diversity and composition of intestinal bacteria (bacterial microbiome) and eukaryotes (eukaryome) are social status and age. In species in which social status determines access to resources, socially dominant animals maintain better immune processes and health status than subordinates. As high species diversity is an index of ecosystem health, the intestinal biome of healthier, socially dominant animals should be more diverse than those of subordinates. Gradual colonization of the juvenile intestine after birth predicts lower intestinal biome diversity in juveniles than adults. We tested these predictions on the effect of: (1) age (juvenile/adult) and (2) social status (low/high) on bacterial microbiome and eukaryome diversity and composition in the spotted hyena (Crocuta crocuta), a highly social, female-dominated carnivore in which social status determines access to resources. We comprehensively screened feces from 35 individually known adult females and 7 juveniles in the Serengeti ecosystem for bacteria and eukaryotes, using a set of 48 different amplicons (4 for bacterial 16S, 44 for eukaryote 18S) in a multi-amplicon sequencing approach. We compared sequence abundances to classical coprological egg or oocyst counts. For all parasite taxa detected in more than six samples, the number of sequence reads significantly predicted the number of eggs or oocysts counted, underscoring the value of an amplicon sequencing approach for quantitative measurements of parasite load. In line with our predictions, our results revealed a significantly less diverse microbiome in juveniles than adults and a significantly higher diversity of eukaryotes in high-ranking than low-ranking animals. We propose that free-ranging wildlife can provide an intriguing model system to assess the adaptive value of intestinal biome diversity for both bacteria and eukaryotes.

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Does lactation lead to resource allocation trade-offs in the spotted hyaena?

Cited by 44 publications

References 76 publications

Reproductive effort influences intra‐seasonal variation in parasite‐specific antibody responses in wild Soay sheep

Reproductive effort influences intra‐seasonal variation in parasite‐specific antibody responses in wild Soay sheep

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

The Intestinal Eukaryotic and Bacterial Biome of Spotted Hyenas: The Impact of Social Status and Age on Diversity and Composition

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