The microbiota influences the Drosophila melanogaster life history strategy

Abstract

AbstractOrganismal life history traits are ideally adapted to local environments when an organism has a fitness advantage in one location relative to conspecifics from other geographies. Local adaptation has been best studied across, for example, latitudinal gradients, where organisms may tradeoff between investment in traits that maximize one, but not both, fitness components of somatic maintenance or reproductive output in the context of finite environmental resources. Latitudinal gradients in life history strategies are traditionally attributed to environmentally mediated selection on an animals genotype, without any consideration of the possible impact of associated microorganisms ( microbiota) on life history traits. Here we show that in Drosophila melanogaster, a key organism for studying local adaptation and life history strategies, associated microorganisms can drive life history variation. First, we reveal that an isogenic fly line reared with different bacteria vary the investment in early reproduction versus somatic maintenance, with little resultant variation in lifetime fitness. Next, we show that in wild Drosophila the abundance of these same bacteria was correlated with the latitude and life history strategy of the flies, and bacterial abundance was driven at least in part by 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; but that the microbiota can override these host genetic adaptations. Taken together, these findings establish the microbiota as an essential consideration in local adaptation and life history evolution.\n\nSignificance statementExplanations of local adaptation have historically focused on how animal genotypes respond to environmental selection. Although the impact of variation in host life histories on the composition of the microbiota has been investigated for many associations, the scale and pattern of microbial effects on host life history strategy are largely unknown. Here we demonstrate in the fruit fly Drosophila melanogaster that microbiota effects on host life history strategy in the laboratory are matched by patterns of microbiota composition in wild host populations. In particular, microbiota composition varies with latitude and the effects of the microbiota on life history traits are greater than host genetic adaptations. Together, these findings demonstrate that the microbiota plays an important role in local adaptation.