Wide-ranging consequences of priority effects governed by an overarching factor

Abstract

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.

Bridging Theory and Experiments of Priority Effects

“…The concepts at the heart of priority effects were first introduced almost a century ago [13], with the term itself being almost half a century old [14]. The term “priority effects” has been subsequently used in many occasions and systems in which this phenomenon has been detected: bacteria and single-cell fungi [3,9,15–17], macroscopic fungi [18,19], protists and planktons [8,20,21], insects [1,5,22], terrestrial plants [2,23], amphibians [4,24] and fish [25,26]. However, these and other studies often differ in the underlying mechanisms and the organizational and temporal scale at which priority effects are measured.…”

“…For instance, in many microbial systems, priority effects are only indirectly inferred by linking changes in community composition to differences in the timing of arrivals; while they are sometimes attributed to factors like resource preemption [27] or phylogenetic relatedness [28,29], the specific mechanisms are often unknown. Other studies in microbial systems point to more resolved mechanisms such as sugar concentration or environmental pH [3,17]. In coral reef fish, priority effects often arise because first arrivers become more aggressive toward later arrivers [25,26,30].…”

Mutational hotspots lead to robust but suboptimal adaptive outcomes in certain environments

“…As the hotspot strain was able to realize and fix the motility-restoring mutation first, it was able to dominate the ecological space. The importance of timing in establishment and survival in a niche is already well known in ecology, where ‘priority effects’ (the sequence of arrival to an environment) determine the outcomes and interactions of groups within that community [8, 54–56]. A similar phenomenon seems to be prevalent here with regard to mutational accessibility; initial establishment seems to be the most important factor for persistence rather than the fitness of the mutation.…”

Intraspecific variation in realized dispersal probability and host quality shape nectar microbiomes

“…Alvarez-P erez & Tsuji & Fukami, 2018;Chappell et al, 2022). However, this line of evidence is contingent on the assumption that Metchnikowia and Acinetobacter are representative of other members of natural communities (Morris et al, 2019) and some habitats may host more diverse nectar microbial communities (e.g.…”

“…Previous work supports the overwhelming dominance of the two microbial genera inoculated in this study in many flowering systems world‐wide (e.g. Álvarez‐Pérez & Herrera, 2013; Tsuji & Fukami, 2018; Chappell et al ., 2022). However, this line of evidence is contingent on the assumption that Metchnikowia and Acinetobacter are representative of other members of natural communities (Morris et al ., 2019) and some habitats may host more diverse nectar microbial communities (e.g.…”