Our understanding of the deterioration in immune function in old age—immunosenescence—derives principally from studies of modern human populations and laboratory animals. The generality and significance of this process for systems experiencing complex, natural infections and environmental challenges are unknown. Here, we show that late-life declines in an important immune marker of resistance to helminth parasites in wild Soay sheep predict overwinter mortality. We found senescence in circulating antibody levels against a highly prevalent nematode worm, which was associated with reduced adult survival probability, independent of changes in body weight. These findings establish a role for immunosenescence in the ecology and evolution of natural populations.
Individual variation in telomere length is predictive of health and mortality risk across a range of species. However, the relative influence of environmental and genetic variation on individual telomere length in wild populations remains poorly understood. Heritability of telomere length has primarily been calculated using parent–offspring regression which can be confounded by shared environments. To control for confounding variables, quantitative genetic “animal models” can be used, but few studies have applied animal models in wild populations. Furthermore, parental age at conception may also influence offspring telomere length, but most studies have been cross‐sectional. We investigated within‐ and between‐parental age at conception effects and heritability of telomere length in the Seychelles warbler using measures from birds caught over 20 years and a multigenerational pedigree. We found a weak negative within‐paternal age at conception effect (as fathers aged, their offspring had shorter telomeres) and a weak positive between‐maternal age at conception effect (females that survived to older ages had offspring with longer telomeres). Animal models provided evidence that heritability and evolvability of telomere length were low in this population, and that variation in telomere length was not driven by early‐life effects of hatch period or parental identities. Quantitative polymerase chain reaction plate had a large influence on telomere length variation and not accounting for it in the models would have underestimated heritability. Our study illustrates the need to include and account for technical variation in order to accurately estimate heritability, as well as other environmental effects, on telomere length in natural populations.
An effective immune response is expected to confer fitness benefits through improved resistance to parasites but also incur energetic costs that negatively impact fitness-related traits, such as reproduction. The fitness costs and benefits of an immune response are likely to depend on host age, sex, and levels of parasite exposure. Few studies have examined the full extent to which patterns of natural selection on immune phenotypes vary across demographic groups and environments in the wild. Here, we assessed natural selection on plasma levels of three functionally distinct isotypes (IgA, IgE, and IgG) of antibodies against a prevalent nematode parasite measured in a wild Soay sheep population over 26 years. We found little support for environment-dependent selection or reproductive costs. However, antibody levels were negatively associated with parasite egg counts and positively associated with subsequent survival, albeit in a highly age-and isotype-dependent manner. Raised levels of antiparasite IgA best predicted reduced egg counts, but this did not predict survival in lambs. In adults increased antiparasite IgG predicted reduced egg counts, and in adult females IgG levels also positively predicted overwinter survival. Our results highlight the potential importance of age-and sex-dependent selection on immune phenotypes in nature and show that patterns of selection can vary even among functionally related immune markers.
Individual variation in telomere length is predictive of health and mortality risk across a range of species. However, the relative influence of environmental and genetic variation on individual telomere length in wild populations remains poorly understood. In previous studies, heritability of telomere length has primarily been calculated using parent-offspring regression, but shared environments can confound such estimates. Furthermore, associations with age and parental age at conception effects are typically not accounted for but can also bias heritability estimates. To control for these confounding variables, quantitative genetic ‘animal models’ can be used. However, the few studies on wild populations using this approach have been restricted by power. Here, we investigated the heritability of telomere length and parental age at conception effects in the Seychelles warbler using 2664 telomere length measures from 1318 birds over 20 years and a multi-generational pedigree. We found a weak negative within-paternal age at conception effect (as fathers aged, their offspring had shorter telomeres) and a weak positive between-maternal age at conception effect (females that survived to older ages had offspring with longer telomeres). While parent–offspring regressions did not detect heritability, animal models provided evidence that heritability of telomere length was low in this population. Environmental and technical variation largely influenced telomere length and would have biased heritability estimates if unaccounted for. Estimating the heritability of telomere length is complex, requiring large sample sizes and accounting for confounding effects in order to improve our understanding of the evolutionary potential of telomere length in the wild.
BackgroundGroup 2 Innate lymphoid cells (ILC2s) are innate cells that produce the TH2 cytokines IL-5 and IL-13. The importance of these cells has recently been demonstrated in experimental models of parasitic diseases but there is a paucity of data on ILC2s in the context of human parasitic infections and in particular of the blood dwelling parasite Schistosoma haematobium.Methodology/Principal FindingsIn this case-control study human peripheral blood ILC2s were analysed in relation to infection with the helminth parasite Schistosoma haematobium. Peripheral blood mononuclear cells of 36 S. haematobium infected and 36 age and sex matched uninfected children were analysed for frequencies of ILC2s identified as Lin-CD45+CD127+CD294+CD161+. ILC2s were significantly lower particularly in infected children aged 6–9 years compared to healthy participants. Curative anti-helminthic treatment resulted in an increase in levels of the activating factor TSLP and restoration of ILC2 levels.ConclusionThis study demonstrates that ILC2s are diminished in young helminth infected children and restored by removal of the parasites by treatment, indicating a previously undescribed association between a human parasitic infection and ILC2s and suggesting a role of ILC2s before the establishment of protective acquired immunity in human schistosomiasis.
Understanding individual variation in fitness‐related traits requires separating the environmental and genetic determinants. Telomeres are protective caps at the ends of chromosomes that are thought to be a biomarker of senescence as their length predicts mortality risk and reflect the physiological consequences of environmental conditions. The relative contribution of genetic and environmental factors to individual variation in telomere length is, however, unclear, yet important for understanding its evolutionary dynamics. In particular, the evidence for transgenerational effects, in terms of parental age at conception, on telomere length is mixed. Here, we investigate the heritability of telomere length, using the ‘animal model’, and parental age at conception effects on offspring telomere length in a wild population of European badgers (Meles meles). Although we found no heritability of telomere length and low evolvability (<0.001), our power to detect heritability was low and a repeatability of 2% across individual lifetimes provides a low upper limit to ordinary narrow‐sense heritability. However, year (32%) and cohort (3%) explained greater proportions of the phenotypic variance in telomere length, excluding qPCR plate and row variances. There was no support for cross‐sectional or within‐individual parental age at conception effects on offspring telomere length. Our results indicate a lack of transgenerational effects through parental age at conception and a low potential for evolutionary change in telomere length in this population. Instead, we provide evidence that individual variation in telomere length is largely driven by environmental variation in this wild mammal.
Offspring from elderly parents often have a lower survival probability because of parental senescence. In cooperatively breeding species, alloparental care provided by helpers is predicted to mitigate age-dependent declines in parental performance. We tested this prediction in the facultatively cooperative-breeding Seychelles warbler (Acrocephalus sechellensis). We find that the provisioning rates of female, but not male, breeders decline sharply with age, and that female breeders reduce their provisioning rates when helpers are present. However, helpers increase the total amount of food provided to the offspring and almost fully compensate for the lower provisioning rates of older female breeders. In territories without helpers, offspring survival declines with age of the female breeder, but not with age of the male breeder, but this decline is counteracted when helpers are present. These results suggest that alloparental care alleviates the costs of senescence for breeders, which may promote cooperative breeding in families with elderly parents.
15Host-parasite interactions are powerful drivers of evolutionary and ecological dynamics in natural 16populations. Variation in immune responses to infection is likely to shape the outcome of these 17 interactions, with important consequences for the fitness of both host and parasite. However, little is 18 known about how genetic variation contributes to variation in immune responses under natural 19 conditions. Here, we examine the genetic architecture of variation in immune traits in the Soay sheep 20 of St Kilda, an unmanaged population of sheep infected with strongyle gastrointestinal nematodes. We 21 assayed IgA, IgE and IgG antibodies against the prevalent nematode Teladorsagia circumcincta in the 22 Author summary 34Host-parasite interactions are powerful drivers of evolutionary and ecological dynamics in natural 35 populations. Variation in immune responses to infection shapes the outcome of these interactions, with 36 important consequences for the ability of the host and parasite to survive and reproduce. However, little 37 is known about how much genes contribute to variation in immune responses under natural conditions. 38Our study investigates the genetic architecture of variation in three antibody types, IgA, IgE and IgG in 39 a wild population of Soay sheep on the St Kilda archipelago in North-West Scotland. Using data 40 collected over 26 years, we show that antibody levels have a heritable basis in lambs and adults and are 41 stable over lifetime of individuals. We also identify several genomic regions with large effects on 42 immune responses. Our study offers the first insights into the genetic control of immunity in a wild 43 population, which is essential to understand how immune profiles vary in challenging natural conditions 44 and how natural selection maintains genetic variation in complex immune traits. 45 46 Studies in humans and livestock have shown that variation in immune traits is often heritable; that is, a 60 significant proportion of phenotypic variance can be attributed to additive genetic effects (4-11). 61Genome-wide association studies (GWAS) in these systems have identified a number of genes of 62 relatively large effect contributing to heritable variation, most notably the major histocompatibility 63 complex (MHC) and cytokine genes (12-17). In wild populations, studies have investigated the 64 heritability of immune traits, most often in birds (18-23), with candidate gene approaches further 65 implicating MHC and cytokine regions in cases where significant associations are observed (23-28). 66However, these studies often focus on broad, non-specific immune phenotypes such as the 67 phytohaemagglutinin (PHA) response, haematocrit levels and/or parasite burden, rather than specific 68 immune responses to ecologically-relevant parasites (29-31). In addition, candidate gene studies focus 69 on a small proportion of the genome and may fail to identify previously undiscovered coding or 70 regulatory regions associated with immune trait variation (32,33). To our knowledge, there...
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