Mosaic selection and gene flow at the onset of grain beetle domestication

Abstract

Domestication is an evolutionary process that can begin before deliberate breeding, when association with humans reshapes gene flow and selection. The yellow mealworm, Tenebrio molitor, is undergoing this transition from a synanthropic pest of stored grain to farmed species. We asked whether gene flow between farmed populations contributes to adaptation to captivity and whether selection extends to production traits. We combined population genomics of 320 beetles from eight farmed and wild populations with genetic mapping of 15 production traits from 3,575 individuals. Farm stocks retained high diversity and weak differentiation, with Netherlands-related ancestry connecting populations across Europe and Canada. Farm-restricted sweep-like signatures were 2.06-fold enriched within regions of excess allele sharing, suggesting local selection on introgressed variation. Across 305 production-trait QTLs, overlaps with selection and introgression signals showed no significant enrichment or depletion, suggesting that adaptive gene flow may primarily contribute to adaptation to captivity rather than broadly shaping growth, development and fertility. Nevertheless, egg-hatching-rate and development-time QTLs overlapped regions of reduced nucleotide diversity and low Tajima's D. These findings support a model in which gene flow supplies variation for unintended selection under intensive rearing. Crowding and physiological stress may favour adaptation to captive environments before sustained breeding establishes a broad genomic response at production loci.