Experimental Removal of Niche Construction Alters the Pace and Mechanisms of Resistance Evolution

Niche construction, a central eco-evolutionary process in which organisms modify their environment, is hypothesised to enhance evolutionary adaptability through feedback between genetic inheritance and the lasting effects of environmental change - known as ecological inheritance. However, while theoretically intriguing, direct empirical support for the effect of niche construction on adaptation is lacking. Red flour beetles modify their environment by releasing quinone-rich stink gland secretions, a form of external immunity. Here, we test in an evolution experiment how experimental removal of niche construction - using RNAi of a key gene needed to produce stink gland secretions - affects the beetles\' adaptation to the bacterial entomopathogen Bacillus thuringiensis. In each generation, beetles inhabited conditioned flour either with regular or drastically reduced stink gland secretion content. Compared to the non-exposed control, all bacteria-exposed regimes rapidly evolved bacterial resistance within only six generations. However, beetles evolving with intact niche construction acquired resistance as soon as after three generations, indicating that adaptation was initially facilitated by niche construction. RNAseq of evolved beetles showed that gene expression differed strongly between the selection regimes, revealing that the mechanisms underlying resistance were dependent on niche construction. Thus, our findings provide urgently needed empirical evidence on the role of niche construction for resistance evolution and its potential genetic basis.