Biological costs and benefits of selective breeding for disease resistance using marker-assisted or field-based selective breeding in honey bees ( Apis mellifera )

Honey bee (Apis mellifera L.) breeders seek to enhance disease resistance by selecting for behavioral resistance traits such as hygienic behavior and Varroa-sensitive hygiene. However, traditional phenotypic assays for these traits are labor-intensive, limiting scalability. Antennal protein biomarkers correlated with these behaviors offer a promising tool for marker-assisted selection (MAS), potentially increasing phenotyping efficiency and accelerating genetic gains. This study evaluated the performance of honey bee colonies from 4 stocks: those selected using field-based phenotypic assays (FAS) or MAS, versus unselected domestic stock (BEN) or imported commercial (IMP) stock. Colonies were situated across 3 distinct geographic regions and were managed with or without acaricide treatment for the treatment of Varroa destructor mites to assess both the benefits of resistance under parasitic stress and potential fitness costs under low-stress conditions. Across regions, MAS and FAS stocks performed comparably in productivity and pathogen metrics and were equal to or more productive than the unselected BEN and IMP stocks. At specific locations and time points, MAS and FAS colonies maintained significantly lower Varroa destructor populations in the absence of acaricides, demonstrating enhanced natural mite suppression. Selection for hygienic behavior was positively associated with colony health and fitness, with no evidence of biologically meaningful trade-offs. Increased overwinter food consumption in selected colonies reflected larger fall populations rather than a direct cost of resistance.