Human-mediated introgression and Varroa destructor shaped the genetic structure of honey bee populations in the Azores.

Abstract

The evolutionary trajectory of island populations can be rapidly altered by human-mediated migration, a process further exacerbated when immigrants introduce invasive parasites, creating new selective pressures. Using customised SNP panels constructed with genome-wide diagnostic loci, we describe the genetic changes in honey bee populations inhabiting the Azores archipelago. As part of a breeding initiative in the 1980s, these populations were recurrently exposed to beekeeper-mediated gene flow from a highly divergent commercial line (C lineage) until the arrival of the Varroa mite to the Azores in 2000, which prompted a honey bee importation ban. Admixture analysis revealed a spatially heterogeneous introgression landscape in the Azores. Four of the five mite-free islands (Santa Maria, São Miguel, Terceira, and São Jorge) presented negligible levels of C-lineage introgression (mean Q-value: 0.004-0.091) despite repeated C-lineage importations in the past. In contrast, the three mite-infested islands (Pico, Faial, and Flores) presented high levels of introgression (mean Q-value: 0.156-0.261). The mite-free island of Graciosa harboured the most admixed population (mean Q-value: 0.392), which is consistent with efforts to eradicate the historical population and replace it with C-lineage honey bees during the implementation of the breeding program. Bayesian inference modelling indicated that the presence of a C-lineage maternal origin and Varroa were associated with increased introgression proportions (100% posterior probability), increasing the mean Q-value by 0.049 and 0.118, respectively. Our findings indicate that these anthropogenic processes altered the historically introduced gene pool and provide a foundation for developing effective conservation strategies to protect honey bees in the Azores.