The microbiota influences the Drosophila melanogaster life history strategy

Abstract

Organisms are locally adapted when members of a population have a fitness advantage in one location relative to conspecifics in other geographies. For example, across latitudinal gradients, some organisms may trade off between traits that maximize fitness components in one, but not both, of somatic maintenance or reproductive output. Latitudinal gradients in life history strategies are traditionally attributed to environmental selection on an animal's genotype, without any consideration of the possible impact of associated microorganisms (“microbiota”) on life history traits. Here, we show in Drosophila melanogaster, a key model for studying local adaptation and life history strategy, that excluding the microbiota from definitions of local adaptation is a major shortfall. First, we reveal that an isogenic fly line reared with different bacteria varies the investment in early reproduction versus somatic maintenance. Next, we show that in wild fruit flies, the abundance of these same bacteria was correlated with the latitude and life history strategy of the flies, suggesting geographic specificity of the microbiota composition. Variation in microbiota composition of locally adapted D. melanogaster could be attributed to both the wild environment and host genetic selection. Finally, by eliminating or manipulating the microbiota of fly lines collected across a latitudinal gradient, we reveal that host genotype contributes to latitude‐specific life history traits independent of the microbiota and that variation in the microbiota can suppress or reverse the differences between locally adapted fly lines. Together, these findings establish the microbiota composition of a model animal as an essential consideration in local adaptation.

Environmental specificity in Drosophila-bacteria symbiosis affects host developmental plasticity

“…Results suggest bacterial treatments influenced host development plastically along the trade-off between speed of development and adult size. This observation echoes recent findings showing that Drosophila bacterial symbionts may induce a trade-off between lifespan and fecundity (Gould et al 2018;Walters et al 2018). On the other hand, our results contrast with previous reports on Drosophila bacterial and yeast symbionts that induce positive relationships between larval and adult traits (Anagnostou et al 2010;Bing et al 2018;Pais et al 2018).…”

“…Second, recent literature shows that the evolution of symbiont transmission depends on which of host's traits it affects (Brown and Akçay 2019); importantly, this mathematical model is based on the plastic trade-off between survival and reproduction. Recent studies have shown that in D. melanogaster bacteria can affect host position along this trade-off (Gould et al 2018;Walters et al 2018). Here, we focused on another tradeoff, the relationship between duration of larval development and adult size at emergence which is well-established in holometabolous insects (Teder et al 2014;Nunney 1996).…”

Common structuring principles of the Drosophila melanogaster microbiome on a continental scale and between host and substrate

“…This is consistent with a model in which genome-wide differentiation of the host populations might also affect loci that interact with the microbiome. Given previous evidence for microbe-interacting loci that vary between natural populations (Corby-Harris and Promislow, 2008; Lazzaro et al, 2008;Behrman et al, 2018;Walters et al, 2020) this seems a reasonable model. Alternatively, the co-structure could be explained by environmental factors that affect both, the microbiome and host genetic variation.…”

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

“…However, we note that contamination would have to differentially affect control and evolved microbiomes to influence our results--which we believe is unlikely. Surveys of microbial diversity in D. melanogaster typically use 16S rRNA profiling and find bacteria from the Acetobacteraceae, Firmicutes, and Enterobacteriaceae [15,17,52]. Our mapping approach detected these bacteria commonly associated with D. melanogaster, but also found abundant methanogens and human commensal microbes (Fig.…”