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Priority effects, where arrival order and initial relative abundance modulate local species interactions, can exert taxonomic, functional, and evolutionary influences on ecological communities by driving them to alternative states. It remains unclear if these wide-ranging consequences of priority effects can be explained systematically by a common underlying factor. Here, we identify such a factor in an empirical system. In a series of field and laboratory studies, we focus on how pH affects nectar-colonizing microbes and their interactions with plants and pollinators. In a field survey, we found that nectar microbial communities in a hummingbird-pollinated shrub, Diplacus (formerly Mimulus ) aurantiacus , exhibited abundance patterns indicative of alternative stable states that emerge through domination by either bacteria or yeasts within individual flowers. In addition, nectar pH varied among D. aurantiacus flowers in a manner that is consistent with the existence of these alternative stable states. In laboratory experiments, Acinetobacter nectaris , the bacterium most commonly found in D. aurantiacus nectar, exerted a strongly negative priority effect against Metschnikowia reukaufii , the most common nectar-specialist yeast, by reducing nectar pH. This priority effect likely explains the mutually exclusive pattern of dominance found in the field survey. Furthermore, experimental evolution simulating hummingbird-assisted dispersal between flowers revealed that M. reukaufii could evolve rapidly to improve resistance against the priority effect if constantly exposed to A. nectaris -induced pH reduction. Finally, in a field experiment, we found that low nectar pH could reduce nectar consumption by hummingbirds, suggesting functional consequences of the pH-driven priority effect for plant reproduction. Taken together, these results show that it is possible to identify an overarching factor that governs the eco-evolutionary dynamics of priority effects across multiple levels of biological organization. 

ABSTRACT Priority effects, where the order and timing of species arrival influence the assembly of ecological communities, have been observed in a variety of taxa and habitats. However, the genetic and molecular basis of priority effects remains unclear, hindering a better understanding of when priority effects will be strong. We sought to gain such an understanding for the nectar yeastMetschnikowia reukaufiicommonly found in the nectar of our study plant, the hummingbird‐pollinatedDiplacus(Mimulus)aurantiacus. In this plant,M.reukaufiican experience strong priority effects when it reaches flowers after other nectar yeasts, such asM.rancensis. After inoculation into two contrasting types of synthetic nectar simulating early arrival ofM.rancensis, we conducted whole‐transcriptome sequencing of 108 strains ofM.reukaufii. We found that several genes were differentially expressed inM.reukaufiistrains when the nectar had been conditioned by growth ofM.rancensis. Many of these genes were associated with amino acid metabolism, suggesting thatM.reukaufiistrains responded molecularly to the reduction in amino acid availability caused byM.rancensis. Furthermore, investigation of expression quantitative trait loci (eQTLs) revealed that genes involved in amino acid transport and resistance to antifungal compounds were enriched in some genetic variants ofM.reukaufii. We also found that gene expression was associated with population growth rate, particularly when amino acids were limited. These results suggest that intraspecific genetic variation in the ability of nectar yeasts to respond to nutrient limitation and direct fungal competition underpins priority effects in this microbial system.