Do yeasts and Drosophila interact just by chance?

Abstract

The fruit fly Drosophila melanogaster and the baker's yeast Saccharomyces cerevisiae are classic research model organisms that are also associated in nature, at least around vineyards. Sharing the same ephemeral fruit niche, winged Drosophila feed on immotile yeasts. That a yeast diet is essential for larvae development and saprophagous fruit flies are attracted to a suite of yeast volatiles has been well established over the last century. Recently, research has focussed on the potential mutual benefit of this interaction hypothesising yeasts also benefit via dispersal from ephemeral fruits. It now appears the concept of a co-evolved mutualism between yeasts and Drosophila has permeated the literature. However, until robust evidence regarding the evolution and maintenance of this yeast-fly association has been provided, we suggest there is no compelling evidence to reject the more simplistic null hypothesis that these interactions are due to exaptation, and not a mutualism driven by natural selection.

Are Drosophila preferences for yeasts stable or contextual?

“…However, it is surprising to find such a high degree of volatile homogeneity across ferments from vastly different horticultural crops, indicating a universal chemical signal for the presence of yeasts. The majority of these YVOCs were tentatively classified as esters (in particular ethyl and acetate esters), fusel‐alcohols, and other intermediates of the Ehrlich‐pathway (Günther & Goddard, ; Hazelwood et al, ). In particular, C 2 /C 3 substituted or branched‐chained volatiles likely resulting from amino acid assimilation were abundant.…”

“…We postulate these interactions may be due to two possible reasons. Firstly, they may be due to exaptation (selection operated on yeast volatile production for other reasons), and that flies have evolved to sense YVOC's to prey on yeasts, in which case specific yeast transfer between fruits by Drosophila and other insects is nothing greater than an fortuitous event, and not one driven by natural selection (Günther & Goddard, ). Alternatively, the ecological reality is that microbes exist as communities (a mix of different individuals and species) in/on fruit (Taylor et al, ), and the concept of a single strain of any microbe metabolizing and emitting volatiles in isolation seems highly unlikely.…”

“…Following this hypothesis, one Saccharomycetaceae cerevisiae isolate (ScNZ) has been shown to derive fitness benefits from interacting with an isofemale D. simulans population, indicating this interaction might comprise a mutualism (Buser et al, ). However, there is evidence that other S. cerevisiae isolates, as well as isolates from other Saccharomycetaceae species, are repulsive to some Drosophila (Buser et al, ; Palanca, Gaskett, Günther, Newcomb, & Goddard, ) , and so it is not yet clear how general or specific any mutualism might be (Günther & Goddard, ). Yeasts produce ethanol which has been shown to induce interference competition with microbes (Goddard, ), but the function of most YVOCs, if indeed they have any other than representing stochastic metabolic endpoints, is not at all well understood (Saerens, Delvaux, Verstrepen, & Thevelein, ).…”

“…Single lines of both, D. simulans and D. melanogaster , were previously described as mutualistic partners for chemically mediated dispersal of S. cerevisiae (Buser et al, ; Christiaens et al, ). It is however not clear whether Drosophila attraction is mediated by a universal YVOCs signal or whether chemically mediated yeast preference is plastic and contextual and thus might arise by chance (Günther & Goddard, ).…”

Advances in the Study of Candida stellata

“…Insects (Drosophila, bees and bumblebees, etc.) act as vectors, and yeasts are an important food source for both the larval and adult stages of numerous insects [5]. Some species of Candida such as C. famata, C. guilliermondii, C. tropicalis, C. parapsilosis, and others may be isolated from natural and polluted water or sediments.…”