A potential role for the gut microbiota in the specialisation of Drosophila sechellia to its toxic host noni (Morinda citrifolia)

Abstract

Adaptation to a novel food source can have significant evolutionary advantages. The fruit fly, Drosophila sechellia, is a specialist of the toxic plant noni (Morinda citrifolia). Little is known as to how D. sechellia has become resistant to the toxins in the fruit - comprised predominantly of octanoic acid - but to date, the behavioural preferences for the fruit and genetic architecture underlying them, have been well studied. Here, we examine whether the gut microbiota could have played a role in adaptation to the fruit. In the first series of experiments, we examine the gut microbiota of wild-type, laboratory reared flies and characterise the gut microbiota when reared on the natural host plant, versus a standard Drosophila diet. We show a rapid transition in the core bacterial diversity and abundance within this species and discover sole precedence of Lactobacillus plantarum when reared on M. citrifolia. We also discover that flies reared on a laboratory diet are more likely to carry bacterial pathogens such as Bacillus cereus, although their function in Drosophila is unknown. Flies reared on a laboratory diet have a significantly reduced weight but with no impact on the risk of death before adulthood, when compared to the wild noni diet. In the second series of experiments, we examine the potential role of the gut microbiota in adaptation to octanoic acid resistance in this species and its sister species, Drosophila melanogaster, to which the fruit is usually fatal. We use a combination of methods to analyse resistance to octanoic acid by conducting life history analysis, behavioural assays and bacterial analysis in both D. sechellia and D. melanogaster. We find that by creating experimental evolution lines of D. melanogaster supplemented with gut microbiota from D. sechellia, we can decrease D. melanogaster aversion to octanoic acid, with the flies even preferring to feed on food supplemented with the acid. We suggest this represents the first step in the evolutionary and ecological specialisation of D. sechellia to its toxic host plant, and that the gut microbiota, Lactobacillus plantarum in particular, may have played a key role in host specialisation.