Temporal variation in the genetic structure of a drone congregation area: an insight into the population dynamics of wild African honeybees (Apis mellifera scutellata)

The mating system of the honeybee ( Apis mellifera ) has been regarded as one of the most panmictic in the animal kingdom, with thousands of males aggregating in drone congregation areas (DCAs) that virgin queens visit to mate with tens of partners. Although males from many colonies gather at such congregations, the temporal changes in the colonies contributing drones remain unknown. Yet, changes in the DCAs' genetic structure will ultimately determine population gene flow and effective population size. By repeatedly sampling drones from an African DCA over a period of 3 years, we studied the temporal changes in the genetic structure of a wild honeybee population. Using three sets of tightly linked microsatellite markers, we were able to reconstruct individual queen genotypes with a high accuracy, follow them through time and estimate their rate of replacement. The number of queens contributing drones to the DCA varied from 12 to 72 and was correlated with temperature and rainfall. We found that more than 80% of these queens were replaced by mostly unrelated ones in successive eight months sampling intervals, which resulted in a clear temporal genetic differentiation of the DCA. Our results suggest that the frequent long-range migration of colonies without nest-site fidelity is the main driver of this high queen turnover. DCAs of African honeybees should thus be regarded as extremely dynamic systems which together with migration boost the effective population size and maintain a high genetic diversity in the population.     

Five hundred and fifty microsatellite markers for the study of the honeybee (Apis mellifera L.) genome

Microsatellites are currently considered the most useful genetic markers with wide applications in genomics, quantitative and population genetics. We present here the structure of the core sequence of 552 microsatellites, together with the sequences of the primers and the length of the sequenced allele. These microsatellites were isolated from several libraries constructed from either fractions of total genomic DNA or from clones of a bacterial artificial chromosome (BAC) library. All 552 loci are polymorphic in the honeybee. Many of them were also successfully amplified in three other species of Apis: A. cerana (58%), A. dorsata (59%) and A. florea (38%). A summary of the variability of 36 loci in the three main evolutionary lineages of A. mellifera is given.     

Reproductive division of labour and thelytoky result in sympatric barriers to gene flow in honeybees (Apis mellifera L.)

Determining the extent and causes of barriers to gene flow is essential for understanding sympatric speciation, but the practical difficulties of quantifying reproductive isolation remain an obstacle to analysing this process. Social parasites are common in eusocial insects and tend to be close phylogenetic relatives of their hosts (= Emery's rule). Sympatric speciation caused by reproductive isolation between host and parasite is a possible evolutionary pathway. Socially parasitic workers of the Cape honeybee, Apis mellifera capensis, produce female clonal offspring parthenogenetically and invade colonies of the neighbouring subspecies A. m. scutellata. In the host colony, socially parasitic workers can become pseudoqueens, an intermediate caste with queenlike pheromone secretion. Here, we show that over an area of approximately 275.000 km2, all parasitic workers bear the genetic signature of a clone founded by a single ancestral worker genotype. Any gene flow from the host to the parasite is impossible because honeybee workers cannot mate. Gene flow from the parasite to the host is possible, as parasitic larvae can develop into queens. However, we show that despite sympatric coexistence for more than a decade, gene flow between host and social parasite (F(st) = 0.32) and hybridizations (0.71%) are rare, resulting in reproductive isolation. Our data suggest a new barrier to gene flow in sympatry, which is not based on assortative matings but on thelytoky and reproductive division of labour in eusocial insects, thereby suggesting a new potential pathway to Emery's rule.