Rapid adaptive evolution of microbial thermal performance curves

Abstract

ABSTRACT Microbial respiration alone releases massive amounts of Carbon (C) into the atmosphere each year, greatly impacting the global C cycle that fuels climate change. Larger microbial population growth often leads to larger standing biomass, which in turns leads to higher respiration. How rising temperatures might influence microbial population growth, however, depends on how microbial thermal performance curves (TPCs) governing this growth may adapt in novel environments. This thermal adaptation will in turn depend on there being heritable genetic variation in TPCs for selection to act upon. While intraspecific variation in TPCs is traditionally viewed as being mostly environmental (E, or plastic) as a single individual can have an entire TPC, our study uncovers substantial heritable genetic variation (G) and Gene-by-Environment interactions (GxE) in the TPC of a widely distributed ciliate microbe. G results in predictable evolutionary responses to temperature-dependent selection that ultimately shape TPC adaptation in a warming world. Through mathematical modeling and experimental evolution assays we also show that TPC GxE leads to predictable temperature-dependent shifts in population genetic makeup that constrains the potential for future adaptation to warming. That is, adaptive evolution can select for decreased genetic variation which subsequently lowers the evolutionary potential of microbial TPCs. Our study reveals how temperature-dependent adaptive evolution shapes microbial population growth, a linchpin of global ecosystem function, amidst accelerating climate warming.