Abstract

With globalization the Western honey bee has become a nearly cosmopolitan species, but it was originally restricted to the Old World. This renowned model of biodiversity has diverged into five evolutionary lineages and several geographic “subspecies.” If Apis mellifera unicolor is indubitably an African subspecies endemic to Madagascar, its relationship with honey bees from three archipelagos in the southwest Indian Ocean (SWIO) hotspot of biodiversity is misunderstood. We compared recent mtDNA diversity data to an original characterization of the nuclear diversity from honey bees in the Mascarenes and Comoros archipelagos, using 14 microsatellites, but also additional mtDNA tRNALeu-cox2 analysis. Our sampling offers the most comprehensive dataset for the SWIO populations with a total of 3,270 colonies from 10 islands compared with 855 samples from Madagascar, 113 from Africa, and 138 from Europe. Comprehensive mitochondrial screening confirmed that honey bees from La Réunion, Mauritius, and Comoros archipelagos are mainly of African origin (88.1% out of 2,746 colonies) and that coexistence with European lineages occurs only in the Mascarenes. PCA, Bayesian, and genetic differentiation analysis showed that African colonies are not significantly distinct on each island, but have diversified among islands and archipelagos. FST levels progressively decreased in significance from European and African continental populations, to SWIO insular and continental populations, and finally among islands from the same archipelago. Among African populations, Madagascar shared a nuclear background with and was most closely related to SWIO island populations (except Rodrigues). Only Mauritius Island presented clear cytoplasmic disequilibrium and genetic structure characteristic of an admixed population undergoing hybridization, in this case, between A. m. unicolor and A. m. ligustica, A. m. carnica and A. m. mellifera-like individuals. Finally, global genetic clustering analysis helped to better depict the colonization and introduction pattern of honey bee populations in these archipelagos.

Highlights

  • Islands are rich reservoirs of biodiversity with high endemism across diverse taxonomic groups [1,2,3]

  • Using the most comprehensive genetic dataset of A. mellifera in the southwest Indian Ocean (SWIO), we propose an interpretation of the intraspecific phylogeographic patterns in the three archipelagos

  • In order to have a comprehensive understanding of SWIO honey bee phylogeography, a dataset containing 1,528 individuals formerly described in Madagascar, Seychelles, Rodrigues, South Africa, and Italy was employed [37] (Table 1)

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Summary

Introduction

Islands are rich reservoirs of biodiversity with high endemism across diverse taxonomic groups [1,2,3]. The islands surrounding Madagascar are part of the Mascarenes Archipelago (La Réunion, Mauritius, and Rodrigues) in the East, the Seychelles Archipelago (Mahé, Praslin, La Digue main islands) in the Northeast and the Comoros Archipelago (Grande Comore, Mohéli, Anjouan, and Mayotte) in the Northwest. In these rich endemic ecosystems, species such as the Western honey bee, Apis mellifera, a generalist pollinator, deserve particular attention.

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