Parasites may severely impact the fitness and life-history of their hosts. After infection, surviving individuals may suppress the growth of the parasite, or completely clear the infection and develop immunity. Consequently, parasite prevalence is predicted to decline with age. Among elderly individuals, immunosenescence may lead to a late-life increase in infection prevalence. We used a 21-year longitudinal dataset from one population of individually-marked Seychelles warblers (Acrocephalus sechellensis) to investigate age-dependent prevalence of the GRW1 strain of the intracellular protozoan blood parasite Haemoproteus nucleocondensus and whether infections with this parasite affect age-dependent survival. We analyzed 2454 samples from 1431 individuals and found that H. nucleocondensus infections could rarely be detected in nestlings. Prevalence increased strongly among fledglings and peaked among older first year birds. Prevalence was high among younger adults and declined steeply until ca 4 years of age, after which it was stable. Contrary to expectations, H. nucleocondensus prevalence did not increase among elderly individuals and we found no evidence that annual survival was lower in individuals suffering from an infection. Our results suggest that individuals clear or suppress infections and acquire immunity against future infections, and provide no evidence for immunosenescence nor an impact of chronic infections on survival.
In small populations, drift results in a loss of genetic variation, which reduces adaptive evolutionary potential. Furthermore, the probability of consanguineous mating increases which may result in inbreeding depression. Under certain circumstances, balancing selection can counteract drift and maintain variation at key loci. Identifying such loci is important from a conservation perspective and may provide insight into how different evolutionary forces interact in small populations. Tolllike receptor (TLR) genes play a pivotal role in vertebrate innate immune defence by recognizing invading pathogens. We characterize TLR variation in the Seychelles warbler (SW) Acrocephalus sechellensis, an endangered passerine that recently suffered a population bottleneck. Five of seven TLR loci were polymorphic, with one locus (TLR15) containing four functional variants and showing an excess of heterozygotes. Haplotype-level tests failed to detect selection at these loci, but site-specific tests detected signatures of positive selection within TLR3 and TLR15. After characterizing variation (excluding TLR15) in 5-6 other Acrocephalus species, we found that TLR variation was positively correlated with population size across species and followed the pattern observed at neutral microsatellite loci. The depauperate TLR variation observed suggests that even at important immunity-related loci, balancing selection may only attenuate the overriding effects of drift. However, in the SW, TLR15 appears to be an outlier and warrants further investigation. The low levels of TLR variation may be disadvantageous for the long-term viability of the SW and conservation measures that maximize the retention of the variation should be considered.
Balancing selection can maintain immunogenetic variation within host populations, but detecting its signal in a postbottlenecked population is challenging due to the potentially overriding effects of drift. Toll-like receptor genes (TLRs) play a fundamental role in vertebrate immune defence and are predicted to be under balancing selection. We previously characterized variation at TLR loci in the Seychelles warbler (Acrocephalus sechellensis), an endemic passerine that has undergone a historical bottleneck. Five of seven TLR loci were polymorphic, which is in sharp contrast to the low genomewide variation observed. However, standard population genetic statistical methods failed to detect a contemporary signature of selection at any TLR locus. We examined whether the observed TLR polymorphism could be explained by neutral evolution, simulating the population's demography in the software DIYABC. This showed that the posterior distributions of mutation rates had to be unrealistically high to explain the observed genetic variation. We then conducted simulations with an agent-based model using typical values for the mutation rate, which indicated that weak balancing selection has acted on the three TLR genes. The model was able to detect evidence of past selection elevating TLR polymorphism in the prebottleneck populations, but was unable to discern any effects of balancing selection in the contemporary population. Our results show drift is the overriding evolutionary force that has shaped TLR variation in the contemporary Seychelles warbler population, and the observed TLR polymorphisms might be merely the 'ghost of selection past'. Forecast models predict immunogenetic variation in this species will continue to be eroded in the absence of contemporary balancing selection. Such 'drift debt' occurs when a gene pool has not yet reached its new equilibrium level of polymorphism, and this loss could be an important threat to many recently bottlenecked populations.
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