Understanding where and how genetic variation is maintained within populations is important from an evolutionary and conservation perspective. Signatures of past selection suggest that pathogen-mediated balancing selection is a key driver of immunogenetic variation, but studies tracking contemporary evolution are needed to help resolve the evolutionary forces and mechanism at play. Previous work in a bottlenecked population of Seychelles warblers (Acrocephalus sechellensis) show that functional variation has been maintained at the viral-sensing Toll-like receptor 3 (TLR3) gene. Here, we characterise evolution at this TLR3 locus over a 25-year period within the original remnant population of the Seychelles warbler, and in four other derived, contained populations. Results show a significant and consistent temporal decline in the frequency of the TLR3C allele in the original population, and that similar declines in the TLR3C allele frequency occurred in all the derived populations. Individuals (of both sexes) with the TLR3CC genotype had lower survival, and males - but not females - that carry the TLR3C allele had significantly lower lifetime reproductive success than those with only the TLR3A allele. These results indicate that positive selection, caused by an as yet unknown agent, is driving TLR3 evolution in the Seychelles warblers. No evidence of heterozygote advantage was detected. However, whether the positive selection observed is part of a longer-term pattern of balancing selection (through fluctuating selection or rare-allele advantage) cannot be resolved without tracking the TLR3C allele in the populations over an extended period of time.

Understanding trade-offs in wild populations is difficult, but important if we are to understand the evolution of life histories and the impact of ecological variables upon them. Markers that reflect physiological state and predict future survival would be of considerable benefit to unravelling such trade-offs and could provide insight into individual variation in senescence. However, currently used markers often yield inconsistent results. One underutilised measure is haematocrit, the proportional of blood comprising of erythrocytes, which relates to the blood’s oxygen-carrying capacity and viscosity, and to individual endurance. Haematocrit has been shown to decline with age in cross-sectional studies (which may be confounded by selective appearance/disappearance). However, few studies have tested whether haematocrit declines within-individuals or whether low haematocrit impacts survival in wild taxa. Using longitudinal data from the Seychelles warbler (Acrocephalus sechellensis), we demonstrated that haematocrit increases with age in young individuals (<1.5 years) but decreases with age in older individuals (1.5–13 years). In breeders, haematocrit was higher in males than females and varied relative to breeding stage. High haematocrit was associated with lower survival in young individuals, but not older individuals. Thus, while we did not find support for haematocrit as a marker of senescence, high haematocrit is indicative of poor condition in younger individuals. Possible explanations are that these individuals were experiencing dehydration and/or high endurance demands prior to capture, which warrants further investigation. Our study demonstrates that haematocrit can be an informative metric for life-history studies investigating trade-offs between survival, longevity and reproduction.