Natural selection on a measure of parasite resistance varies across ages and environmental conditions in a wild mammal (original) (raw)
Related papers
Fitness costs of parasites explain multiple life history tradeoffs in a wild mammal
2019
A longstanding prediction of life history theory states that parasitism can provide a mechanistic link between current and future fitness, thereby mediating life history tradeoffs. Demonstrating this mechanism in the wild involves linking a reproductive cost for parasitism with a cost of parasitism for fitness, which requires high-resolution longitudinal monitoring of individuals. Here, we examined associations among reproductive investment, immunity, parasitism, and fitness-related traits in a wild population of individually identified red deer (Cervus elaphus). Using path analysis, we constructed and analysed possible links among these traits, particularly investigating whether costs of lactation for survival and fecundity were likely to act through increased parasitism. Lactation was associated with increased strongyle parasitism, which was then associated with decreased subsequent fitness for all four fitness-related traits we examined. In addition, lactation was directly associ...
Parasitology, 2010
Maternal effects occur when the maternal phenotype influences that of the offspring in addition to the effects of maternal genes, and may have a considerable influence on offspring parasite resistance. These effects, and the effects of early levels of reproduction and parasite resistance, may persist into later life and even influence ageing rates. Here we analyse a 20-year longitudinal data set collected on a free-living population of Soay sheep, to investigate the associations between a suite of maternal phenotypic traits and early-life performance on measures of parasite resistance across life. Our results show that maternal effects are important in determining offspring parasite resistance, since lambs born as twins and those born to the youngest and oldest mothers show higher parasite burdens. We show that the association between parasite resistance and natal litter size persists into adulthood. We also show that age-specific changes in parasite resistance in males are associated with natal litter size, and that age-specific changes in females are influenced by early-life levels of reproduction and parasite infection. These results add to the growing evidence that conditions experienced by individuals during development can have a profound influence on immediate and late-life performance and may even influence ageing.
Effect of selection for productive traits on internal parasite resistance in sheep
Host resistance to internal parasites, as measured by faecal e ggcountanddagginess wasinvestigatedinramiambs borninthe 1981-83 years (approximately generation 3) from the Woodlands selection lines. Lines were selected for either: number of lambs born, 100 day weight, hogget fleece weight and a production index in which all three traits are combined; a fifth line was a randomly selected control. Ramlambs were drenched withanthelmintic and thenexposed to contaminatedpasture foraperiodof 6-7 weeks and then faecal sampled. Total plasma protein, albumin and pepsinogen were measured. The results demonstrated significant variation between selection lines in faecal egg count, dag score, liveweight gain, wool growth and blood plasma parameters. Between selection lines, faecal egg count was positively correlated with liveweight gain (0.95) and wool growth (0.41). Blood pepsinogen and total blood protein were both negatively associated with faecal egg count and liveweight gain (correlations of-0.51 to-0.90). Using sire variation within selection line (progeny of 65 sires), produced heritability estimates of 0.13 f 0.07 and 0.25 f 0.09 for strong~~e and Nemafodirus faecal egg count respectively. Significant positive genetic correlations between strongyle faecal egg count and hogget fleece weight were observed.
Genetically resistant sheep avoid parasites to a greater extent than do susceptible sheep
Proceedings. Biological sciences / The Royal Society, 2007
Livestock breeding programmes have created resistant (R) and susceptible (S) sheep that differ in their ability to control parasites through their immune function but potentially also their grazing behaviour (i.e. parasite avoidance). Using the Perendale genetic lines, we tested the hypothesis that R-sheep avoid parasites more effectively, reducing their parasite exposure/challenge, compared with S-sheep. However, in grazing systems, parasite-rich areas are also forage rich, suggesting that parasite avoidance behaviours are associated with nutritional penalties. We first created a naturally heterogeneous sward structure of gaps and tussocks and then used focal behavioural observations to quantify the sward selection of R- and S-sheep. Tussock swards were more nitrogen rich (41%), offered increased forage intake rates (32%) and contained 17 times more parasite larvae than gap swards. All the animals avoided grazing the tussock swards. However, the R-sheep grazed the tussock swards to...
Hosts and parasites co-evolve, with each lineage exerting selective pressures on the other. Thus, parasites may influence host life-history characteristics, such as longevity, and simultaneously host life-history may influence parasite diversity. If parasite burden causes increased mortality, we expect a negative association between host longevity and parasite species richness. Alternatively, if long-lived species represent a more stable environment for parasite establishment, host longevity and parasite species richness may show a positive association. We tested these two opposing predictions in carnivores, primates and terrestrial ungulates using phylogenetic comparative methods and controlling for the potentially confounding effects of sampling effort and body mass. We also tested whether increased host longevity is associated with increased immunity, using white blood cell counts as a proxy for immune investment. Our analyses revealed weak relationships between parasite species richness and longevity. We found a significant negative relationship between longevity and parasite species richness for ungulates, but no significant associations in carnivores or primates. We also found no evidence for a relationship between immune investment and host longevity in any of our three groups. Our results suggest that greater parasite burden is linked to higher host mortality in ungulates. Thus, shorter-lived ungulates may be more vulnerable to disease outbreaks, which has implications for ungulate conservation, and may be applicable to other shortlived mammals.
Proceedings of the Royal Society B: Biological Sciences, 2009
Despite widespread empirical evidence for a general deterioration in the majority of traits with advancing age, it is unclear whether the progress of senescence is chronologically determined, or whether factors such as environmental conditions experienced over the lifespan are more important. We explored the relative importance of 'chronological' and 'environmental' measures of age to changes in parasite resistance across the lifespan of free-living Soay sheep. Our results show that individuals experience an increase in parasite burden, as indicated by gastrointestinal helminth faecal egg count (FEC) with chronological age. However, chronological age fails to fully explain changes in FEC because a measure of environmental age, cumulative environmental stress, predicts an additional increase in FEC once chronological age has been accounted for. Additionally, we show that in females age-specific changes are dependent upon the environmental conditions experienced across individuals' life histories: increases in FEC with age were greatest among individuals that had experienced the highest degree of stress. Our results illustrate that chronological age alone may not always correspond to biological age, particularly in variable environments. In these circumstances, measures of age that capture the cumulative stresses experienced by an individual may be useful for understanding the process of senescence.
Ecology and evolution, 2016
Immune defenses are expected to be crucial for survival under the considerable parasite pressures experienced by wild animals. However, our understanding of the association between immunity and fitness in nature remains limited due to both the complexity of the vertebrate immune system and the often-limited availability of immune reagents in nonmodel organisms. Here, we use methods and reagents developed by veterinary researchers for domestic ungulates on blood samples collected from a wild Soay sheep population, to evaluate an unusually broad panel of immune parameters. Our evaluation included different innate and acquired immune cell types as well as nematode parasite-specific antibodies of different isotypes. We test how these markers correlate with one another, how they vary with age-group and sex, and, crucially, whether they predict overwinter survival either within or among demographic groups. We found anticipated patterns of variation in markers with age, associated with imm...
Reproduction has different costs for immunity and parasitism in a wild mammal
Life history theory predicts that reproductive investment draws resources away from immunity, resulting in increased parasitism. However, studies of reproductive tradeoffs rarely examine multiple measures of reproduction, immunity, and parasitism. It is therefore unclear whether the immune costs of reproductive traits correlate with their resource costs, and whether increased parasitism emerges from weaker immunity. We examined these relationships in wild female red deer (Cervus elaphus) with variable reproductive investment and longitudinal data on mucosal antibody levels and helminth parasitism. We noninvasively collected faecal samples, counting propagules of strongyle nematodes (order: Strongylida), the common liver fluke Fasciola hepatica and the red deer tissue nematode Elaphostrongylus cervi. We also quantified both total and anti-strongyle mucosal IgA to measure general and specific immune investment. Contrary to our predictions, we found that gestation was associated with d...
Natural selection on individual variation in tolerance of gastrointestinal nematode infection
2014
Hosts may mitigate the impact of parasites by two broad strategies: resistance, which limits parasite burden, and tolerance, which limits the fitness or health cost of increasing parasite burden. The degree and causes of variation in both resistance and tolerance are expected to influence host-parasite evolutionary and epidemiological dynamics and inform disease management, yet very little empirical work has addressed tolerance in wild vertebrates. Here, we applied random regression models to longitudinal data from an unmanaged population of Soay sheep to estimate individual tolerance, defined as the rate of decline in body weight with increasing burden of highly prevalent gastrointestinal nematode parasites. On average, individuals lost weight as parasite burden increased, but whereas some lost weight slowly as burden increased (exhibiting high tolerance), other individuals lost weight significantly more rapidly (exhibiting low tolerance). We then investigated associations between tolerance and fitness using selection gradients that accounted for selection on correlated traits, including body weight. We found evidence for positive phenotypic selection on tolerance: on average, individuals who lost weight more slowly with increasing parasite burden had higher lifetime breeding success. This variation did not have an additive genetic basis. These results reveal that selection on tolerance operates under natural conditions. They also support theoretical predictions for the erosion of additive genetic variance of traits under strong directional selection and fixation of genes conferring tolerance. Our findings provide the first evidence of selection on individual tolerance of infection in animals and suggest practical applications in animal and human disease management in the face of highly prevalent parasites.
Journal of animal …, 2004
Fecal egg count (FEC) has been widely used as an indicator of host resistance to gastrointestinal parasites in sheep and has been shown to be a heritable trait. Two other possible indicators of parasites, dag score (DS; accumulated fecal material) and fecal consistency score (FCS), were investigated in this study, along with BW. All four traits were studied to see how heritability and genetic correlations varied with age from weaning (4 mo) to hogget age (approximately 400 d). More than 1,100 lambs, the offspring of 37 rams, were recorded eight times between weaning (3 to 5 mo of age) and hogget age (13 to 18 mo of age) on two farms. Sire models were fitted to the data from each trait at each recording and in a repeatability model involving the whole data set. Overall, the heritabilities were 0.28 ± 0.072 (FEC), 0.11 ± 0.036 (DS), 0.12 ± 0.036 (FCS), and 0.23 ± 0.070 (BW).