Are you my mother? When host genetics and gut microbiota tell different phylogenetic stories in the Africanized honey bee hybrid (Apis mellifera scutellata × sspp.)

ABSTRACT Africanized honey bees (Apis mellifera scutellata × sspp.) originated in Brazil through the crossbreeding of African (A. mellifera scutellata) and European (A. mellifera sspp.) honey bee subspecies. African genes came to dominate in these hybrid honey bees over time. Gut microbiota co-evolve with their hosts and generally reflect host phylogeny. To examine if this was true in Africanized honey bee hybrids (also known as scutellata-European hybrids), we compared the gut microbiota (16S rRNA) of three honey bee subspecies: African, European, and Africanized bees. Publicly available sequencing data from five honey bee studies were downloaded from the National Center for Biotechnology Information (NCBI). European bee samples (n = 42) came from the United Kingdom, Switzerland, and the United States. African bee samples (n = 82) came from Kenya. Africanized bee samples (n = 10) came from Brazil. Unexpectedly, Africanized honey bee gut microbiota was far more similar to European bees than to African bees despite the closer host genetic relationship between African and Africanized bees. All three subspecies shared similar relative abundances of core taxa. We posit that the similarity in gut microbiota between Africanized and European honey bees arose from the nature of the crossbreeding and the social/environmental transmission of gut microbiota within hives. Namely, African queens took over European hives. However, the hybrid offspring acquired their gut microbiota from European nurse bees and European hive materials, resulting in the stable transmission of European gut microbiota across generations. Our results provide an intriguing insight into the potential ecological, social, and environmental factors that shape the gut microbiota of the Africanized honey bee hybrid.IMPORTANCEAfricanized honey bee hybrids originated in Brazil through the crossbreeding of African and European honey bee subspecies. In this study, we examined the gut microbiota of all three honey bee subspecies (African, European, Africanized). A few core microbiota were shared across all subspecies. Interestingly, while African honey bee genes dominated in the Africanized honey bee hybrids, their gut microbial composition was most similar to European bees. This is likely related to the way these bees were crossbred—with African queens taking over European hives, while gut microbial inoculation of hybrids came from European nurse bees and European hive materials. Gut microbiota are critical to honey bee health, and studying the gut microbiota of closely related honey bee subspecies helps understand the factors that influence gut microbial composition. This is important for our broader understanding of honey bee health, conservation, and evolution.