Tolerance of liver fluke infection varies between breeds and producers in beef cattle.

Liver flukes (Fasciola spp.) are important helminth parasites of livestock globally and cause substantial reductions in health and productivity of beef cattle. Attempts to control fluke have been thwarted by the difficulty of vaccine design, the evolution of flukicide resistance and the need to control the intermediate snail host. Mechanisms to reduce the impact of parasites on animal performance have typically focused on promoting host resistance - defined as the ability of the host to kill and remove the parasite from its system - and such strategies include improving protein nutrition or selective breeding for resistance. Organisms, however, have another broad mechanism for mitigating the impact of parasites: they can show tolerance, defined as the ability to maintain health or performance under increasing parasite burden. Tolerance has been studied in the plant literature for over a century, but there are very few empirical studies of parasite tolerance in livestock. In this study, we used data collected from >90 000 beef cattle to estimate the impact of the severity of liver fluke infection on performance and variation in tolerance of fluke. Severity of liver fluke infection was estimated using liver "fibrosis score" on a scale of 0-3 and performance estimated as (1) age at slaughter and (2) daily dead weight gain. Animals with higher fibrosis scores were slaughtered around 2 weeks later than animals with no fluke and gained around 10 g less weight per day. There was also considerable variation in these effects of fibrosis score, such that animals from different producers and breeds varied in their tolerance of fluke infection. While breeds did not vary in the association between fibrosis and age at slaughter, there was considerable variation among producers: high fibrosis score delayed slaughter by up to 50 days in some producers, but not at all in others. Meanwhile, there was support for variation in the slope of daily dead weight gain on fibrosis score among both breeds and producers, with some unaffected by high fluke scores and some breeds and producers experiencing a 20 g/day lower weight gain under high fluke scores. Our results point to the potential for both environmental and genetic variation in tolerance of liver fluke in cattle, paving the way for quantitative genetic and nutritional research into the feasibility of promoting tolerance as a disease mitigation strategy.

Early reproductive investment, senescence and lifetime reproductive success in female Asian elephants.

The evolutionary theory of senescence posits that as the probability of extrinsic mortality increases with age, selection should favour early-life over late-life reproduction. Studies on natural vertebrate populations show early reproduction may impair later-life performance, but the consequences for lifetime fitness have rarely been determined, and little is known of whether similar patterns apply to mammals which typically live for several decades. We used a longitudinal dataset on Asian elephants (Elephas maximus) to investigate associations between early-life reproduction and female age-specific survival, fecundity and offspring survival to independence, as well as lifetime breeding success (lifetime number of calves produced). Females showed low fecundity following sexual maturity, followed by a rapid increase to a peak at age 19 and a subsequent decline. High early life reproductive output (before the peak of performance) was positively associated with subsequent age-specific fecundity and offspring survival, but significantly impaired a female's own later-life survival. Despite the negative effects of early reproduction on late-life survival, early reproduction is under positive selection through a positive association with lifetime breeding success. Our results suggest a trade-off between early reproduction and later survival which is maintained by strong selection for high early fecundity, and thus support the prediction from life history theory that high investment in reproductive success in early life is favoured by selection through lifetime fitness despite costs to later-life survival. That maternal survival in elephants depends on previous reproductive investment also has implications for the success of (semi-)captive breeding programmes of this endangered species.

Causes and consequences of intra- and inter-host heterogeneity in defence against nematodes.

Despite strong natural and artificial selection for increased resistance to nematode parasites, there is considerable heterogeneity between hosts in human, livestock and wildlife populations, with a minority of hosts carrying the majority of parasites. In addition, levels of defence may vary across the lifespan of individuals due to changes in their physiological state and infection history. Such variation influences nematode transmission dynamics and the evolution of parasite life-history strategies. Therefore, identifying sources of between- and within-individual variation in resistance and predicting their consequences is crucial for understanding the epidemiology of nematode parasitic diseases. In this review, several key sources of variation are identified, using examples from mouse models, immuno-epidemiological studies of human populations and observational and experimental studies of wildlife and livestock. The mutual applicability of approaches used across these study systems is emphasized, with the assertion that the concerted efforts of researchers from a range of disciplines will enable us to better understand the proximate and ultimate causes of variation in defence against nematode parasites. This will facilitate predictions of the epidemiological and evolutionary consequences of this variation, with the potential to improve disease treatment and management.

Detecting genes for variation in parasite burden and immunological traits in a wild population: testing the candidate gene approach.

Identifying the genes underlying phenotypic variation in natural populations can provide novel insight into the evolutionary process. The candidate gene approach has been applied to studies of a number of traits in various species, in an attempt to elucidate their genetic basis. Here, we test the application of the candidate gene approach to identify the loci involved in variation in gastrointestinal parasite burden, a complex trait likely to be controlled by many loci, in a wild population of Soay sheep. A comprehensive literature review, Gene Ontology databases, and comparative genomics resources between cattle and sheep were used to generate a list of candidate genes. In a pilot study, these candidates, along with 50 random genes, were then sequenced in two pools of Soay sheep; one with low gastrointestinal nematode burden and the other high, using a NimbleGen sequence capture experiment. Further candidates were identified from single nucleotide polymorphisms (SNPs) that were highly differentiated between high- and low-resistance sheep breeds. A panel of 192 candidate and control SNPs were then typed in 960 individual Soay sheep to examine whether they individually explained variation in parasite burden, as measured as faecal egg count, as well as two immune measures (Teladorsagia circumcincta-specific antibodies and antinuclear antibodies). The cumulative effect of the candidate and control SNPs were estimated by fitting genetic relationship matrices (GRMs) as random effects in animal models of the three traits. No more significant SNPs were identified in the pilot sequencing experiment and association study than expected by chance. Furthermore, no significant difference was found between the proportions of candidate or control SNPs that were found to be significantly associated with parasite burden/immune measures. No significant effect of the candidate or control gene GRMs was found. There is thus little support for the candidate gene approach to the identification of loci explaining variation in parasitological and immunological traits in this population. However, a number of SNPs explained significant variation in multiple traits and significant correlations were found between the proportions of variance explained by individual SNPs across multiple traits. The significant SNPs identified in this study may still, therefore, merit further investigation.

Natural selection on a measure of parasite resistance varies across ages and environmental conditions in a wild mammal.

Parasites detrimentally affect host fitness, leading to expectations of positive selection on host parasite resistance. However, as immunity is costly, host fitness may be maximized at low, but nonzero, parasite infection intensities. These hypotheses are rarely tested on natural variation in free-living populations. We investigated selection on a measure of host parasite resistance in a naturally regulated Soay sheep population using a longitudinal data set and found negative correlations between parasite infection intensity and annual fitness in lambs, male yearlings and adult females. However, having accounted for confounding effects of body weight, the effect was only significant in lambs. Associations between fitness and parasite resistance were environment-dependent, being strong during low-mortality winters, but negligible during harsher high-mortality winters. There was no evidence for stabilizing selection. Our findings reveal processes that may shape variation in parasite resistance in natural populations and illustrate the importance of accounting for correlated traits in selection analysis.

Maternal effects and early-life performance are associated with parasite resistance across life in free-living Soay sheep.

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.

The serological incidence of Hypoderma bovis in cattle in England and Wales in spring 1989.

Sera from 152,434 cattle held on 6175 farms in England and Wales were tested for the presence of antibodies to Hypoderma bovis during the 10 weeks starting on February 6, 1989. Thirty-nine positive animals (25.6 animals/100,000 tested) were identified on 21 of the farms (0.34 per cent). In comparison, the survey in 1988 examined 74,502 cattle on 3087 farms and found 29 positive animals (38.9/100,000 tested) on 18 farms (0.58 per cent).