Resistance evolution driven by niche construction – the role of microbiota and beetle secretions

Through niche construction, organisms actively shape their environment, thereby influencing their evolutionary trajectories via ecological inheritance. Red flour beetles ( Tribolium castaneum ) achieve niche construction through secretion of antimicrobial compounds from the stink glands. It has recently been demonstrated that the experimental removal of niche construction using RNAi of a key gene needed to produce stink gland secretions altered the pace and mechanisms of resistance adaptation to the bacterial entomopathogen Bacillus thuringiensis within nine host generations. However, it is unknown whether the microbiome and secretions produced by beetles undergo changes during experimental evolution. We continued the evolution experiment with an additional nine generations of selection. We found that host resistance continued to increase in selection regimes with pathogen exposure, whereas host development and fecundity remained stable, thereby confirming our previous findings. We then profiled larvae-associated microbiota in generations 12 and 15 via 16S rRNA sequencing and measured the stink gland secretion profiles of adults via gas chromatography-flame ionization detection in generation 18. While adaptation to the pathogen did not affect the microbiota, lines evolving with the possibility to construct their niches showed increased microbial diversification, and chemical secretion profiles did not change in either of the selection regimes. Together, our results highlight the role of niche construction in shaping host–microbe interactions. These effects seemed to be independent of any microevolutionary changes in the secretions as a niche-constructing trait.