National Wildlife Management Centre, Animal and Plant Health Agency, Stonehouse, UK.
Centre for Ecology and Conservation, University of Exeter, Penryn, UK.
J Anim Ecol. 2018 Nov;87(6):1500-1511. doi: 10.1111/1365-2656.12878. Epub 2018 Jul 20.
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.
衰老的突变积累理论预测，当近亲繁殖导致有害等位基因纯合时，与年龄相关的适应性恶化可能会被夸大。在自然种群中，适应度的一个重要组成部分是疾病的发病率和进展。越来越多的证据表明，近亲繁殖与衰老之间、与疾病之间、与性别之间以及与疾病之间存在自然联系。然而，迄今为止，在单一自然种群中，还几乎没有证据表明年龄、疾病、近亲繁殖和性别之间存在联系。利用长期纵向实地研究的生态和流行病学数据，我们表明，在自然暴露于牛结核病（bTB）的野生欧洲獾（Meles meles）中，近亲繁殖（以多位点纯合度衡量）加剧了年龄与进展性感染证据之间的正相关关系（以对 bTB 的抗体反应衡量），但仅在雌性中。雄性獾的年龄与进展性感染之间的关系比雌性更为陡峭，而近亲繁殖状态没有影响。我们发现，在两性的生命早期，近亲繁殖与进展性感染的发生率之间没有联系。我们的研究结果强调了年龄相关的近亲繁殖对与健康相关的特征（疾病状态）的影响在雌性中增加。这种关系与衰老的突变积累理论的预测一致，但也可能存在其他机制。例如，通过除突变积累以外的机制导致的晚年条件下降，可能会增加晚年近亲繁殖衰退的幅度。无论哪种机制导致了观察到的模式，我们都表明，近亲繁殖会影响与年龄相关的疾病模式，并且可以扩展到影响特征为衰老的适应度成分的晚年下降的幅度和时间。更好地理解近亲繁殖、疾病和衰老之间的性别特异性联系，可以深入了解种群水平的病原体动态，并可能影响对人畜共患病野生动物宿主的管理策略。
