Abstract
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.
Highlights
Parasites and their mammalian hosts have complex and dynamic relationships (Bush, Fernández, Esch, & Seed, 2001; Irvine, 2006; Knowles et al, 2013; Lello, Boag, Fenton, Stevenson, & Hudson, 2004) with long joint evolutionary histories (Hafner & Nadler, 1988)
Consistent with evidence that immune processes in juvenile mammals improve with age, both Ancylostoma (Table 2) and Cystoisospora (Table 3) loads decreased as juveniles increased in age
One plausible explanation could be an encounter‐reduction effect whereby adult hyenas reduce the chance of juveniles encountering Ancylostoma infective larvae
Summary
Parasites and their mammalian hosts have complex and dynamic relationships (Bush, Fernández, Esch, & Seed, 2001; Irvine, 2006; Knowles et al, 2013; Lello, Boag, Fenton, Stevenson, & Hudson, 2004) with long joint evolutionary histories (Hafner & Nadler, 1988). High‐ranking individuals in mammalian groups typically have greater access to food resources and a higher nutritional status than low‐ranking individuals, and as a result, offspring reared by high‐ranking mothers are often better nourished than those reared by low‐ranking mothers (Clutton‐Brock & Huchard, 2013; Hofer, Benhaiem, Golla, & East, 2016) This suggests that juveniles reared by high‐ranking mothers (high‐ranking juveniles) should find it easier to allocate the energy and protein (Jones et al, 2011) required for the maintenance of effective immune processes and the repair of parasite damaged tissue than those reared by low‐ranking mother (low‐ranking juveniles). Higher resistance is expected in high‐ranking than low‐ranking juveniles and in older than younger juveniles. (c) The transmission of Cystoisospora by the fecal–oral route during social contacts predicts higher infection loads in high‐ranking than low‐ranking juveniles, if resistance to infection is similar in these rank categories. (d) Environmental contamination with both Ancylostoma and Cystoisospora infective stages is expected to increase as the number of clan members increases, thereby elevating infection loads. (e) The energetic cost of high infection loads of either Ancylostoma or Cystoisospora should compromise immune responses, thereby increasing the number of coinfecting taxa. (f) we expect the survival of young juvenile hyenas to adulthood and their longevity to decrease with increasing Ancylostoma and/or Cystoisospora infection loads, and the fitness cost of high infection loads to be less in high‐ranking juveniles than low‐ranking juveniles, that is, we expect high‐ranking juveniles to be more tolerant of high infection loads
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