Shahmohamadloo René S, Gabidulin Amir R, Andrews Ellie R, Rudman Seth M
bioRxiv. 2025 Jul 2:2025.06.27.661976. doi: 10.1101/2025.06.27.661976.
Understanding how populations adapt to environmental change is a central goal in evolutionary biology. Microbiomes have been proposed as a source of heritable variation that is central to rapid adaptation in hosts, yet empirical evidence supporting this remains limited, particularly in naturalistic settings. We combined a field evolution experiment in exposed to an insecticide with microbiome manipulations to disentangle the contributions of host standing genetic variation and microbiome evolution to adaptation. Within three generations, independent populations rapidly and repeatedly evolved increased survivorship, a defining feature of resistance evolution. Adaptive changes in sub-lethal traits such as reproductive output, stress tolerance, and body size occurred with a delayed response following the evolution of resistance. Core microbiome taxa declined following insecticide exposure, and resistant populations evolved to house lower microbial abundances. Axenic rearing and microbiome transplant experiments demonstrated that adaptation via host standing genetic variation was the mechanism for resistance evolution. Microbiome evolution played a secondary and cryptic role in host adaptation by masking slowed development rates that evolved in resistant populations. Together, these results reinforce the primacy of adaptation occurring through selection on host standing genetic variation while also demonstrating the contributions of microbiome evolution in host adaptation.
Identifying the mechanisms that allow organisms to adapt to environmental stress is a foundational goal in biology. Using field experimental evolution and microbiome manipulations in , we directly tested the relative contributions of host genomic evolution and microbiome evolution to adaptation. We found that adaptation to environmental stress occurred rapidly and repeatedly, driven primarily by selection on host standing genetic variation, with microbiome evolution acting as a secondary contributor. These findings reinforce the importance of host genetic variation in rapid adaptation and demonstrate that microbiome evolution can contribute to host evolutionary trajectories in a cryptic manner.
了解种群如何适应环境变化是进化生物学的核心目标。微生物组被认为是可遗传变异的一个来源，对宿主的快速适应至关重要，然而支持这一观点的实证证据仍然有限，尤其是在自然环境中。我们将一项在暴露于杀虫剂环境下的田间进化实验与微生物组操作相结合，以厘清宿主固有遗传变异和微生物组进化对适应的贡献。在三代之内，独立的种群迅速且反复地进化出了更高的存活率，这是抗性进化的一个决定性特征。在抗性进化之后，诸如繁殖输出、应激耐受性和体型等亚致死性状的适应性变化出现了延迟反应。接触杀虫剂后，核心微生物组分类群减少，抗性种群进化为具有较低的微生物丰度。无菌饲养和微生物组移植实验表明，通过宿主固有遗传变异进行的适应是抗性进化的机制。微生物组进化在宿主适应中发挥了次要且隐秘的作用，它掩盖了抗性种群中进化出的发育速率减缓现象。总之，这些结果强化了通过对宿主固有遗传变异进行选择而发生适应的首要地位，同时也证明了微生物组进化在宿主适应中的贡献。
确定生物体适应环境压力的机制是生物学的一个基本目标。通过在[具体物种]中进行田间实验进化和微生物组操作，我们直接测试了宿主基因组进化和微生物组进化对适应的相对贡献。我们发现，对环境压力的适应迅速且反复地发生，主要由对宿主固有遗传变异的选择驱动，微生物组进化起次要作用。这些发现强化了宿主遗传变异在快速适应中的重要性，并表明微生物组进化可以以隐秘的方式对宿主进化轨迹做出贡献。
