USA honey bee populations display restrictions in their mtDNA haplotype diversity

Authors: Alburaki, Mohamed; Madella, Shayne; Lopez, Jillian; BOUGA, MARIA - Agricultural University Of Athens; Chen, Yanping - Judy; VAN ENGELSDORP, DENNIS - University Of Maryland

Submitted to: Frontiers in Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/1/2022
Publication Date: 1/4/2023
Citation: Alburaki, M., Madella, S., Lopez, J.A., Bouga, M., Chen, Y., Van Engelsdorp, D. 2023. USA honey bee populations display restrictions in their mtDNA haplotype diversity. Frontiers in Genetics. 13:1092121. https://doi.org/10.3389/fgene.2022.1092121.
DOI: https://doi.org/10.3389/fgene.2022.1092121

Interpretive Summary: As a non-native species, the honey bee genetic stock in the USA is limited by the import of genetics from the Old World. A healthy genetic diversity within honey bee populations is critical to provide tolerance and resistance to current and future diseases and predators. Honey bees have been suffering high losses over the last decade, emphasizing the need to understand what drives these losses. Lack of genetic diversity has been suggested as one such cause. This study provides a comprehensive and unprecedented analysis of the genetic diversity of the honey bee populations in the USA. It details and validates the methodology used to transit a widely used mtDNA genetic marker in honey bees from its traditional way to a more precise and systemic in silico test which therefore eliminates discrepancies and reconciles haplotype identities between various investigations. This work identified and named a total of fifteen novel haplotypes of three honey bee evolutionary lineages that have never been reported before, providing new insights into the evolutionary history of the USA’s honey bees since their importation to North America in the 1600s. Finally, from the perspective of national importance, the low haplotype diversity and the overwhelming reliance on two mtDNA haplotypes of the same lineage are all alarming signals of the existence of poor maternal genetic backgrounds and heredity within the honey bee populations of the USA.

Technical Abstract: The genetic diversity of the USA’s honey bee (Apis mellifera L.) populations was examined by molecular approach using two mitochondrial (mtDNA) markers. A total of 1,063 samples were analyzed for the mtDNA intergenic region located between the cytochrome c oxidase I & II (COI-COII) and 401 samples were investigated for the NADH dehydrogenase 2 (ND2) coding gene. The samples represented 45 states, the District of Colombia and two territories of the USA. Nationwide, three maternal evolutionary lineages were identified: the North Mediterranean lineage C (93.79%), the West Mediterranean lineage M (3.2%) and the African lineage A (3.01%). A total of 27 haplotypes were identified, 13 of them (95.11%) were already reported and 14 others (4.87%) were found to be novel haplotypes that are exclusive to the USA. The number of haplotypes per state/territory ranged between two and eight and the haplotype diversity H ranged between 0.236 - 0.763 with a nationwide haplotype diversity of 0.597. Furthermore, the honey bee populations of the USA were shown to rely heavily (76.64%) on two single haplotypes (C1=38.76%, C2j=37.62%) of the same lineage characterizing A. m. ligustica and A. m. carnica subspecies, respectively. Molecular-variance parsimony in COI-COII and ND2 confirmed this finding and underlined the central and ancestral position of C2d within the C lineage. Moreover, major haplotypes of A. m. mellifera (M3a, M7b, M7c) were recorded in six states (AL, AR, HI, MO, NM and WA). Four classic African haplotypes (A1e, A1v, A4, A4p) were also identified in nine states and Puerto Rico, with higher frequencies in southern states like LA, FL and TX. This data suggests an urgent need to enhance the maternal genetic diversity of the US honey bee populations.