Microbiome science has provided groundbreaking insights into human and animal health. Similarly, evolutionary medicine – the incorporation of eco-evolutionary concepts into primarily human medical theory and practice – is increasingly recognised for its novel perspectives on modern diseases. Studies of host–microbe relationships have been expanded beyond humans to include a wide range of animal taxa, adding new facets to our understanding of animal ecology, evolution, behaviour, and health. In this review, we propose that a broader application of evolutionary medicine, combined with microbiome science, can provide valuable and innovative perspectives on animal care and conservation. First, we draw on classic ecological principles, such as alternative stable states, to propose an eco-evolutionary framework for understanding variation in animal microbiomes and their role in animal health and wellbeing. With a focus on mammalian gut microbiomes, we apply this framework to populations of animals under human care, with particular relevance to the many animal species that suffer diseases linked to gut microbial dysfunction (e.g. gut distress and infection, autoimmune disorders, obesity). We discuss diet and microbial landscapes (i.e. the microbes in the animal's external environment), as two factors that are (i) proposed to represent evolutionary mismatches for captive animals, (ii) linked to gut microbiome structure and function, and (iii) potentially best understood from an evolutionary medicine perspective. Keeping within our evolutionary framework, we highlight the potential benefits – and pitfalls – of modern microbial therapies, such as pre- and probiotics, faecal microbiota transplants, and microbial rewilding. We discuss the limited, yet growing, empirical evidence for the use of microbial therapies to modulate animal gut microbiomes beneficially. Interspersed throughout, we propose 12 actionable steps, grounded in evolutionary medicine, that can be applied to practical animal care and management. We encourage that these actionable steps be paired with integration of eco-evolutionary perspectives into our definitions of appropriate animal care standards. The evolutionary perspectives proposed herein may be best appreciated when applied to the broad diversity of species under human care, rather than when solely focused on humans. We urge animal care professionals, veterinarians, nutritionists, scientists, and others to collaborate on these efforts, allowing for simultaneous care of animal patients and the generation of valuable empirical data.

中文翻译：

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将微生物组科学和进化医学融入动物健康和保护

微生物组科学为人类和动物健康提供了开创性的见解。同样，进化医学——将生态进化概念纳入主要的人类医学理论和实践——因其对现代疾病的新颖视角而日益受到认可。对宿主与微生物关系的研究已经扩展到人类以外的范围，包括广泛的动物分类单元，为我们对动物生态、进化、行为和健康的理解增加了新的方面。在这篇综述中，我们建议更广泛地应用进化医学，与微生物组科学相结合，可以为动物护理和保护提供有价值和创新的观点。首先，我们利用经典的生态原理，例如替代稳定状态，提出一个生态进化框架，用于理解动物微生物组的变化及其在动物健康和福祉中的作用。我们以哺乳动物肠道微生物组为重点，将该框架应用于人类护理下的动物群体，特别是与患有与肠道微生物功能障碍相关的疾病（例如肠道窘迫和感染、自身免疫性疾病、肥胖）的许多动物物种。我们讨论饮食和微生物景观（即动物外部环境中的微生物），作为两个因素（i）代表圈养动物的进化不匹配，（ii）与肠道微生物组结构和功能相关，以及（iii）潜在的从进化医学的角度最好地理解。在我们的进化框架内，我们强调现代微生物疗法的潜在好处和陷阱，例如益生菌和益生菌、粪便微生物群移植和微生物野化。我们讨论了使用微生物疗法有益地调节动物肠道微生物组的有限但不断增长的经验证据。我们提出了 12 个基于进化医学的可行步骤，可应用于实际的动物护理和管理。我们鼓励将这些可行的步骤与生态进化观点结合到我们对适当动物护理标准的定义中。本文提出的进化观点在应用于人类照顾下的广泛多样性物种时可能会得到最好的理解，而不是仅仅关注人类。我们敦促动物护理专业人员、兽医、营养师、科学家和其他人在这些努力上进行合作，以便同时护理动物患者并生成有价值的经验数据。