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

Abstract

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.

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

“…For Ancylostoma duodenale , fecundity (the number of eggs/g feces per worm) is density‐dependent, declining from 287 eggs to approximately 100 eggs for the first 100 worms and then remains largely independent thereafter (Anderson & Schad, ); hence, FECs are a reasonable index of adult worm infection load. Also, Heitlinger et al () found a significant positive correlation between egg or oocyst counts and the amount of parasite DNA in the feces for the taxa identified as Ancylostoma , Diphyllobothrium, and Coccidia in this study population. In pigs, Trichuris suis egg counts are deemed a reliable approximate estimate of the number of adult worms per host, that is, parasite load (Gassó et al, ).…”

“…This suggests the intriguing idea that the fitness cost of a more diverse GI parasite community may be lower than one dominated by a limited number of taxa. Previously, we found that the eukaryome in high‐ranking hyenas is more diverse than that of low‐ranking animals (Heitlinger et al, ) which may indicate that high‐ranking animals have a more diverse, stable, and ecologically “healthy” GI community than low‐ranking animals.…”

“…We determined fecal egg counts (FECs, eggs/g feces) and fecal oocyst counts (FOCs, oocysts/g feces) as previously described (East et al, 2015;Heitlinger et al, 2017) using the McMaster egg flotation technique following Foreyt (2001). We screened 2 g of feces per sample and used a potassium iodide (KI) solution with a specific weight of 1.5 g/ml and with a dilution ratio of 1:15 (Meyer-Lucht & Sommer, 2005).…”

“…Parasites and their mammalian hosts have complex and dynamic relationships (Bush, Fernández, Esch, & Seed, ; Irvine, ; Knowles et al, ; Lello, Boag, Fenton, Stevenson, & Hudson, ) with long joint evolutionary histories (Hafner & Nadler, ). Wild mammals are typically infected with a taxonomically diverse range of gastrointestinal (GI) macroparasites and microparasites, and individuals vary considerably in their infection loads and diversity of coinfecting parasite taxa (Heitlinger, Ferreira, Thierer, Hofer, & East, ; Irvine, Stien, Halvorsen, Langvatn, & Albon, ; MacIntosh, Hernandez, & Huffman, ; Seltmann, Webster, Ferreira, Czirják, & Wachter, ). This heterogeneity is thought to be shaped by interactions between numerous factors associated with the host, the infecting parasite(s), and the environment.…”

“…A range of intestinal parasites infect wild spotted hyenas ( Crocuta crocuta ) (Baylis, ; Berentsen et al, ; East et al, ; Engh et al, ; Graber & Blanc, ), and recently, a metabarcoding study extended knowledge on the composition and diversity of the bacterial microbiome and eukaryome in this species (Heitlinger et al, ). Spotted hyenas (hereafter termed hyenas) are social carnivores that live in multifemale, multimale fission–fusion societies termed clans (Kruuk, ) that defend territories (Frank, ).…”