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Gut microbiomes and reproductive isolation in Drosophila

Significance The evolutionary significance of assortative mating by diet, mediated by gut bacteria is a puzzle, but it has had a huge impact and has provided a keystone to support increasing interest in the “holobiome.” However, in species such as Drosophila melanogaster that have flexible gut microbiomes, any reproductive isolation mediated by gut bacteria specific to host diets can only be transient. Here, we replicated and extended tests of this idea. Despite differences in gut microbiomes, we failed to recover previously observed patterns of nonrandom mating and found no evidence that mating preferences were associated with diet or gut bacteria. This suggests that the evolutionary importance of gut microbiomes in host divergence needs careful consideration on a case-by-case basis. Experimental studies of the evolution of reproductive isolation (RI) in real time are a powerful way in which to reveal fundamental, early processes that initiate divergence. In a classic speciation experiment, populations of Drosophila pseudoobscura were subjected to divergent dietary selection and evolved significant positive assortative mating by diet. More recently, a direct role for the gut microbiome in determining this type of RI in Drosophila melanogaster has been proposed. Manipulation of the diet, and hence the gut microbiome, was reported to result in immediate assortative mating by diet, which could be eliminated by reducing gut microbes using antibiotics and recreated by adding back Lactobacillus plantarum. We suggest that the evolutionary significance of this result is unclear. For example, in D. melanogaster, the microbiome is reported as flexible and largely environmentally determined. Therefore, microbiome-mediated RI would be transient and would break down under dietary variation. In the absence of evolutionary coassociation or recurrent exposure between host and microbiome, there are no advantages for the gut bacteria or host in effecting RI. To explore these puzzling effects and their mechanisms further, we repeated the tests for RI associated with diet-specific gut microbiomes in D. melanogaster. Despite observing replicable differences in the gut microbiomes of flies maintained on different diets, we found no evidence for diet-associated RI, for any role of gut bacteria, or for L. plantarum specifically. The results suggest that there is no general role for gut bacteria in driving the evolution of RI in this species and resolve an evolutionary riddle.