Contrasting effects of nectar yeasts on the reproduction of Mediterranean plant species

Abstract

Premise Yeasts are often present in floral nectar and can influence plant fitness directly (independently of pollinators) or indirectly by influencing pollinator visitation and behavior. However, few studies have assessed the effect of nectar yeasts on plant reproductive success or compared effects across different plant species, limiting our understanding of the relative impact of direct vs. indirect effects. Methods We inoculated the nectar of six plant species in the field with the cosmopolitan yeast Metschnikowia reukaufii to analyze the direct and indirect effects on female reproductive success over 2 years. The pollinator assemblage for each species was recorded during both flowering years. Results Direct yeast effects on female fecundity were statistically nonsignificant for all plant species. There were significant indirect, pollinator‐mediated effects on fruit production and seed mass for the two species pollinated almost exclusively by bumblebees or hawkmoths, with the direction of the effects differing for the quantity‐ and quality‐related fitness components. There were no consistent effects of the yeast on maternal fecundity for any of the species with diverse pollinator assemblages. Conclusions Effects of M. reukaufii on plant reproduction ranged from negative to neutral or positive depending on the plant species. The among‐species variation in the indirect effects of nectar yeasts on plant pollination could reflect variation in the pollinator community, the specific microbes colonizing the nectar, and the order of microbial infection (priority effects), determining potential species interactions. Elucidating the nature of these multitrophic plant–pollinator–microbe interactions is important to understand complex processes underlying plant pollination.

Nature’s Most Fruitful Threesome: The Relationship between Yeasts, Insects, and Angiosperms

“…Finally, de Vega et al [ 142 ] have recently reported that the effects of M. reukaufii on the reproduction of different Mediterranean plants ranged from negative to neutral or positive, depending on the plant species. Moreover, the authors suggested that the inter-species variation in the indirect effects of nectar-inhabiting yeasts on plant pollination might be due to the variation in the pollinator community, the specific microbes colonizing floral nectar, and the order of microbial arrival to the nectary (i.e., priority effects) [ 142 ]. Therefore, the differences between treatments observed by these authors might be driven not only by the interaction of M. reukaufii with insect pollinators, but also by the interactions of this yeast species with other nectar microbes, such as bacteria [ 142 ].…”

Dispersal overwhelms variation in host quality to shape nectar microbiome assembly

“…Alternatively, non-pathogenic floral microbes are common (Vannette, 2020). In floral nectar, bacteria or yeasts may affect plant fitness via changes to floral phenotype that change pollinator visitation (Vannette et al ., 2012; Schaeffer et al ., 2017; Vannette & Fukami, 2018), shift pollinators’ on-flower behavior (Herrera et al ., 2013; de Vega et al ., 2022), or by competing with or facilitating other beneficial, commensal, and pathogenic microbes (Crowley-Gall et al ., 2022; Mueller et al ., 2022). Compared to the microbiomes of leaves or roots, floral microbiomes are highly variable among flowers on a plant, among individual plants, and among plant species (Rebolleda-Gómez et al ., 2019; Vannette, 2020).…”

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

“…Our study system here consists of the bacteria and yeasts that colonize the floral nectar of the sticky monkeyflower, Diplacus (formerly Mimulus ) aurantiacus , a hummingbird-pollinated shrub native to California and Oregon of the USA ( Belisle et al, 2012 ). Initially sterile, floral nectar is colonized by these microbes via pollinator-mediated dispersal ( Belisle et al, 2012 ; de Vega et al, 2022 ). Microbial communities that develop in nectar through this dispersal are often simple, dominated by one or a few species of nectar-specialist bacteria or yeast ( Álvarez-Pérez et al, 2019 ; Golonka and Vilgalys, 2013 ; Herrera et al, 2010 ; Tsuji and Fukami, 2018 ; Warren et al, 2020 ).…”

“…Together, the stochastic dispersal and the history-dependent interactions jointly cause priority effects in nectar microbial communities. Moreover, recent studies indicate that whether flowers are dominated by bacteria or yeasts can affect pollination and seed set, although a mechanism for this effect remains unclear ( de Vega et al, 2022 ; Good et al, 2014 ; Herrera et al, 2013 ; Jacquemyn et al, 2021 ; Junker et al, 2014 ; Rering et al, 2020 ; Schaeffer and Irwin, 2014 ; Vannette et al, 2013 ; Vannette and Fukami, 2016 ; Yang et al, 2019 ). Despite the increasing amount of knowledge about this system, whether or not there is a common factor that explains the various phenomena associated with priority effects has not been investigated in this system, or any other system for that matter, to our knowledge.…”