UNLABELLED

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.

SIGNIFICANCE

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.