Experimental evolution of insect resistance to two pesticide classes reveals mechanistic diversity and context-dependent fitness costs

Abstract

Does rapid adaptation to stressors evolve through similar underlying mechanisms among diverse populations, or are there many roads to a similar phenotype? The experimental evolution of pesticide resistance in insects provides a powerful model to study the diverse evolutionary signatures of adaptation and their associated costs. Here, we selected for resistance to two pesticides (organophosphates and pyrethroids) in six field-derived populations of the red flour beetle (Tribolium castaneum). After several generations of selection, we performed transcriptomic analyses and measured survival, development, and fecundity in the presence and absence of pesticides to detect fitness costs of resistance evolution. All pesticide-selected populations exhibited significantly improved survival after pesticide exposure without substantial fitness costs, compared to control populations. Populations that evolved to resist organophosphates had distinct gene expression in the presence and absence of organophosphates, supporting different detoxification mechanisms and cuticular modifications among populations. In contrast, pyrethroid resistant populations demonstrated common differential expression of cytochrome P450 transcripts. Furthermore, some populations evolved similar mechanisms against both pesticides while others showed little overlap in their evolved responses, suggesting variation in potential cross-resistance phenotypes. Overall, between populations, we observed both parallel and divergent patterns in gene expression associated with acquired pesticide resistance, without ubiquitous fitness costs.