Bacterial Adaptation to the Host's Diet Is a Key Evolutionary Force Shaping Drosophila-Lactobacillus Symbiosis

Abstract

SummaryAnimal-microbe facultative symbioses play a fundamental role in ecosystem and organismal health. Yet, due to the flexible nature of their association, the selection pressures that act on animals and their facultative symbionts remain elusive. Here we apply experimental evolution to Drosophila melanogaster associated with its growth-promoting symbiont Lactobacillus plantarum, representing a well-established model of facultative symbiosis. We find that the diet of the host, rather than the host itself, is a predominant driving force in the evolution of this symbiosis. Furthermore, we identify a mechanism resulting from the bacterium's adaptation to the diet, which confers growth benefits to the colonized host. Our study reveals that bacterial adaptation to the host's diet may be the foremost step in determining the evolutionary course of a facultative animal-microbe symbiosis.

Meta-analysis suggests the microbiome responds to Evolve and Resequence experiments inDrosophila melanogaster

“…While this is the first examination of the microbiome in the E&R context, other studies have implicated the microbiome in host adaptation in D. melanogaster. For example, when flies are monoassociated with Lactobacillus plantarum in nutrient poor environments, L. plantarum rapidly evolved symbiotic benefits to increase fly fitness [45]. Across replicates, the de novo appearance of several SNPs in the acetate kinase gene (ackA) in L. plantarum promoted larval growth and nutrition, and subsequently, this L. plantarum variant increased in frequency across fly generations.…”

Can the microbiome influence host evolutionary trajectories?

“…To best match phenotype to local environment, hosts may use microbial variation to alter developmental timing. Development in many taxa, from insects [107][108][109][110][111][112][113] to plants [114][115][116] to crustaceans 117,118 , changes in response to microbial variation. Developmental plasticity, through microbial variation, may expose novel phenotypic variation 119 , and this may in turn generate phenotypes that allow rapid acclimation to variable environments.…”

“…Above, we identified common scenarios of how the microbiome may influence host evolutionary processes. To provide more mechanistic insight into host-microbiome evolutionary processes, experimental evolution can provide a powerful approach to understand how microbial change interacts with host evolution 14,113,122 . However, few studies have actually explicitly evaluated evolutionary responses in the microbiome.…”

“…And how frequently does the host utilize this rapid microbial evolution? A recent study, where the temporal evolutionary dynamics were monitored, suggests that Lactobacillus bacteria in Drosophila evolve rapidly to nutrient poor diets, and Drosophila can leverage rapid microbial adaptation independent of their own evolution 113 . More experiments are needed that combine genotyping and phenotyping host-microbiome interactions to understand the temporal evolutionary dynamics.…”

Continent-wide structure of bacterial microbiomes of European Drosophila melanogaster suggests host-control

“…As in mammals and other organisms, environmental factors, such as the time of collection Adair et al, 2018) or diet (Chandler et al, 2011;Staubach et al, 2013;Erkosar et al, 2018;Wang and Staubach, 2018) have a strong effect on the Drosophila microbiome. The food-substrate that flies live on can be a more important driver of adaptation for the microbes than the host environment in D. melanogaster (Martino et al, 2018).…”