Dispersal enhances beta diversity in nectar microbes

Abstract

Dispersal is considered a key driver of beta diversity, the variation in species composition among local communities, but empirical tests remain limited. We manipulated dispersal of nectar-inhabiting bacteria and yeasts via flower-visiting animals to examine how dispersal influenced microbial beta diversity among flowers. Contrary to the prevailing view that dispersal lowers beta diversity, we found beta diversity was highest when dispersal was least limited. Our analysis suggested that this unexpected pattern might have resulted from stronger priority effects under increased dispersal. Dispersal is highly stochastic, generating variability in species arrival history and consequently the potential for community divergence via priority effects, in these and likely many other microbial, plant, and animal communities. Yet most previous experiments eliminated this possibility. We suggest that the positive effects of dispersal on beta diversity, like the one we report here, may have been greatly underappreciated.

Floral organs act as environmental filters and interact with pollinators to structure the yellow monkeyflower (Mimulus guttatus) floral microbiome

“…In general, we would expect dispersal to homogenize communities across distance (Vellend, ). However, similar to what we observed here, pollinator‐mediated dispersal of nectar microbes has been shown to decrease beta‐diversity in Mimulus aurantiacus (Vannette & Fukami, ). There are different reasons why beta diversity might increase with dispersal.…”

“…While it is often assumed that pollinators play a key role in dispersal of microbial communities, and some systems bear this out (e.g., yeast nectar communities; Pozo, Herrera, & Alonso, ; Vannette & Fukami, ), insects visiting flowers have diverse interactions with organs within a flower (Plowright & Laverty, ). In this study, pollinator treatment on its own did not account for differences in community composition, but rather affected the importance of organ selection in explaining differences in community composition across samples.…”

“…Thus, understanding the relative contributions of drift (i.e., neutral) and selective processes in the host can provide insight on the drivers of host‐associated microbiome assembly, their changes over time (e.g., Burns et al, ), and the potential sources of these microbes (e.g., Venkataraman et al, ). Recently, flower‐associated microbiomes have been established as an excellent system to study community assembly and metacommunity dynamics (Belisle, Peay, & Fukami, ; Chappell & Fukami, ; Shade, McManus, & Handelsman, ; Vannette & Fukami, ).…”

“…Despite significant variation across floral organs, and potential effects of microbes of anthers, pollen, styles and stigma on direct fitness effects (not mediated by pollinators), most studies of microbial communities associated with flowers have concerned microbes of nectar (e.g., Belisle et al, ; Herrera et al, ; Mittelbach, Yurkov, Stoll, & Begerow, ; Pozo et al, ; Vannette & Fukami, ). These studies have shown the importance of pollinators in shaping some of the assembly patterns of these microbiomes (Belisle et al, ; Herrera et al, ; Vannette & Fukam, ). However, there is substantial variation in microbial composition that is not explained by the presence/absence of pollinators (e.g., Vannette & Fukami, ), and the source of most floral microbes remains unknown (even after including other floral organs, Figure ).…”

“…These studies have shown the importance of pollinators in shaping some of the assembly patterns of these microbiomes (Belisle et al, ; Herrera et al, ; Vannette & Fukam, ). However, there is substantial variation in microbial composition that is not explained by the presence/absence of pollinators (e.g., Vannette & Fukami, ), and the source of most floral microbes remains unknown (even after including other floral organs, Figure ). Each floral organ is likely to create unique conditions for the establishment of bacteria (Aleklett, Hart, & Shade, ; Junker & Keller, ).…”