Chappell, C. R. | Search bioRxiv

bioRxiv2024

Transcriptional responses to priority effects in nectar yeast

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 in most cases, hindering the mechanistic understanding of priority effects. We sought to gain such understanding for the common nectar yeast Metschnikowia reukaufii, which engages in strong priority effects with other species of nectar yeast, including M. rancensis, another species commonly found in the nectar of our study plant, the hummingbird-pollinated Diplacus (Mimulus) aurantiacus. After inoculation into two contrasting types of synthetic nectar simulating early arrival of M. rancensis, we conducted whole-transcriptome sequencing of 108 genetically diverse strains of M. reukaufii. We found that several genes were differentially expressed in M. reukaufii strains when the nectar had been conditioned by growth of M. rancensis. Many of these genes were associated with amino acid metabolism, consistent with our previous finding that early-arriving species limit late-arriving species growth by reducing amino acid availability. Furthermore, investigation of expression quantitative trait loci (eQTLs) revealed that genes involved in amino acid transport and resistance to antifungal compounds were enriched in genetic variants, with differing effects on gene expression based on priority effects of M. rancensis. These results demonstrate that intraspecific variation in the ability of nectar yeasts to respond to nutrient limitation and direct fungal competition may underpin the molecular mechanisms of priority effects.

ecology↗

bioRxiv2022

pH as an eco-evolutionary driver of priority effects

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 aurantiacus, exhibited patterns indicative of alternative stable states through domination by either bacteria or yeasts within individual flowers. 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.

ecology↗