Survival costs of reproduction are mediated by parasite infection in wild Soay sheep

Abstract

A trade‐off between current and future fitness potentially explains variation in life‐history strategies. A proposed mechanism behind this is parasite‐mediated reproductive costs: individuals that allocate more resources to reproduction have fewer to allocate to defence against parasites, reducing future fitness. We examined how reproduction influenced faecal egg counts (FEC) of strongyle nematodes using data collected between 1989 and 2008 from a wild population of Soay sheep in the St. Kilda archipelago, Scotland (741 individuals). Increased reproduction was associated with increased FEC during the lambing season: females that gave birth, and particularly those that weaned a lamb, had higher FEC than females that failed to reproduce. Structural equation modelling revealed future reproductive costs: a positive effect of reproduction on spring FEC and a negative effect on summer body weight were negatively associated with overwinter survival. Overall, we provide evidence that parasite resistance and body weight are important mediators of survival costs of reproduction.

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

“…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, ).…”

“…Our analyses revealed that changes in FEC across the season were influenced by reproductive effort: females that reproduced ( Figure 3, Supporting Information Table S1) and those that produced heavier litters (Figure 2b, 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, 2019), bighorn sheep Ovis canadensis (Festa-Bianchet, 1989), domestic…”

“…Associations between FEC and different antibody isotypes were complex and suggested that strongyle‐specific IgG exerts a protective effect, but that total IgM may reflect exposure to infection. This adds to a growing body of evidence in the Soay sheep linking reproductive effort, strongyle‐specific antibodies, strongyle FEC and survival (Gulland, ; Hayward et al, ; Nussey et al, ; Tempest, ; Watt et al, Leivesley et al, ) which suggest that the peri‐parturient relaxation of immunity (PPRI) is likely to have downstream consequences for parasite transmission and host fitness. There is profound variation between individuals in how FEC and immune responses change during reproduction, which is by no means all explained by reproductive effort.…”

“…The PPR is largely a consequence of protein deficit due to the heavy nutritional demands of reproduction (Donaldson, Houtert, & Sykes, 2001), which mean that fewer resources are available to mount parasite-specific antibody responses, which are diminished in pregnant and lactating ewes (Beasley, Kahn, & Windon, 2010,2012. The PPR has also been documented in the wild population of Soay sheep living in the remote St Kilda archipelago (Tempest, 2005;Wilson, Grenfell, Pilkington, Boyd, & Gulland, 2004), with recent work showing that females that successfully raised a lamb to weaning had a more pronounced PPR than those that failed to wean a lamb and, as a consequence, reduced survival Leivesley et al (2019). The degree to which changes in strongylespecific immune responses during reproduction can explain the PPR in Soay sheep has not, however, been established.…”

Fitness costs of parasites explain multiple life history tradeoffs in a wild mammal

“…The deer are not amenable to experimental manipulation, but they are censused regularly, providing detailed information on their survival and reproductive success (Clutton-Brock et al ., 1982). In such situations, path analysis can be used to infer links between parasites and their fitness consequences (Pacejka et al ., 1998; Stjernman et al ., 2004; Brambilla et al ., 2015; Leivesley et al ., 2019). Notably, a recent analysis in a wild population of Soay sheep used path analysis to demonstrate that reproduction reduced survival through increased parasite intensity and reduced body weight (Leivesley et al ., 2019).…”