Abstract
The mutation accumulation theory of senescence predicts that age-related deterioration of fitness can be exaggerated when inbreeding causes homozygosity for deleterious alleles. A vital component of fitness, in natural populations, is the incidence and progression of disease. Evidence is growing for natural links between inbreeding and ageing; between inbreeding and disease; between sex and ageing; and between sex and disease. However, there is scant evidence, to date, for links among age, disease, inbreeding and sex in a single natural population. Using ecological and epidemiological data from a long-term longitudinal field study, we show that in wild European badgers (Meles meles) exposed naturally to bovine tuberculosis (bTB), inbreeding (measured as multilocus homozygosity) intensifies a positive correlation between age and evidence of progressed infection (measured as an antibody response to bTB), but only among females. Male badgers suffer a steeper relationship between age and progressed infection than females, with no influence of inbred status. We found no link between inbreeding and the incidence of progressed infection during early life in either sex. Our findings highlight an age-related increase in the impact of inbreeding on a fitness-relevant trait (disease state) among females. This relationship is consistent with the predictions of the mutation accumulation theory of senescence, but other mechanisms could also play a role. For example, late-life declines in condition, arising through mechanisms other than mutation accumulation might have increased the magnitude of inbreeding depression in late life. Whichever mechanism causes the observed patterns, we have shown that inbreeding can influence age-dependent patterns of disease and, by extension, is likely to affect the magnitude and timing of the late-life declines in components of fitness that characterise senescence. Better understanding of sex-specific links between inbreeding, disease and ageing provides insights into population-level pathogen dynamics and could influence management strategies for wildlife reservoirs of zoonotic disease.
Highlights
| INTRODUCTIONInbreeding depression describes a reduction in the fitness of offspring of related individuals (Charlesworth & Charlesworth, 1987; Darwin, 1876; Slate et al, 2004) and is explained by the expression of deleterious alleles that are made homozygous by breeding among related individuals
Using ecological and epidemiological data from a long-term longitudinal field study, we show that in wild European badgers (Meles meles) exposed naturally to bovine tuberculosis, inbreeding intensifies a positive correlation between age and evidence of progressed infection, but only among females
Inbreeding depression describes a reduction in the fitness of offspring of related individuals (Charlesworth & Charlesworth, 1987; Darwin, 1876; Slate et al, 2004) and is explained by the expression of deleterious alleles that are made homozygous by breeding among related individuals
Summary
Inbreeding depression describes a reduction in the fitness of offspring of related individuals (Charlesworth & Charlesworth, 1987; Darwin, 1876; Slate et al, 2004) and is explained by the expression of deleterious alleles that are made homozygous by breeding among related individuals. The badger system is well suited to the study of links between age, sex and inbreeding, because age-related declines in immune cell telomere length and cytokine responses have been documented in both sexes (Beirne, Delahay, Hares, & Young, 2014; Beirne et al, 2016), and sex differences in components of immunity have been reported (Beirne et al, 2016) Evidence of both reproductive (Dugdale, Pope, Newman, Macdonald, & Burke, 2011) and body mass senescence (Beirne, Delahay, & Young, 2015) have been documented. We propose that this link between inbreeding and age-d ependent patterns of infection will differ between males and females, but it is difficult to predict which sex will suffer age-dependent progression more acutely, or in which sex it will be most detected
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