A Single SNP Turns a Social Honey Bee (Apis mellifera) Worker into a Selfish Parasite.

The evolution of altruism in complex insect societies is arguably one of the major transitions in evolution and inclusive fitness theory plausibly explains why this is an evolutionary stable strategy. Yet, workers of the South African Cape honey bee (Apis mellifera capensis) can reverse to selfish behavior by becoming social parasites and parthenogenetically producing female offspring (thelytoky). Using a joint mapping and population genomics approach, in combination with a time-course transcript abundance dynamics analysis, we show that a single nucleotide polymorphism at the mapped thelytoky locus (Th) is associated with the iconic thelytokous phenotype. Th forms a linkage group with the ecdysis-triggering hormone receptor (Ethr) within a nonrecombining region under strong selection in the genome. A balanced detrimental allele system plausibly explains why the trait is specific to A. m. capensis and cannot easily establish itself into genomes of other honey bee subspecies.

The transcriptomic changes associated with the development of social parasitism in the honeybee Apis mellifera capensis.

Social insects are characterized by the division of labor. Queens usually dominate reproduction, whereas workers fulfill non-reproductive age-dependent tasks to maintain the colony. Although workers are typically sterile, they can activate their ovaries to produce their own offspring. In the extreme, worker reproduction can turn into social parasitism as in Apis mellifera capensis. These intraspecific parasites occupy a host colony, kill the resident queen, and take over the reproductive monopoly. Because they exhibit a queenlike behavior and are also treated like queens by the fellow workers, they are so-called pseudoqueens. Here, we compare the development of parasitic pseudoqueens and social workers at different time points using fat body transcriptome data. Two complementary analysis methods-a principal component analysis and a time course analysis-led to the identification of a core set of genes involved in the transition from a social worker into a highly fecund parasitic pseudoqueen. Comparing our results on pseudoqueens with gene expression data of honeybee queens revealed many similarities. In addition, there was a set of specific transcriptomic changes in the parasitic pseudoqueens that differed from both, queens and social workers, which may be typical for the development of the social parasitism in A. m. capensis.

Genome-wide analysis of signatures of selection in populations of African honey bees (Apis mellifera) using new web-based tools.

BACKGROUND: With the development of inexpensive, high-throughput sequencing technologies, it has become feasible to examine questions related to population genetics and molecular evolution of non-model species in their ecological contexts on a genome-wide scale. Here, we employed a newly developed suite of integrated, web-based programs to examine population dynamics and signatures of selection across the genome using several well-established tests, including F ST, pN/pS, and McDonald-Kreitman. We applied these techniques to study populations of honey bees (Apis mellifera) in East Africa. In Kenya, there are several described A. mellifera subspecies, which are thought to be localized to distinct ecological regions. RESULTS: We performed whole genome sequencing of 11 worker honey bees from apiaries distributed throughout Kenya and identified 3.6 million putative single-nucleotide polymorphisms. The dense coverage allowed us to apply several computational procedures to study population structure and the evolutionary relationships among the populations, and to detect signs of adaptive evolution across the genome. While there is considerable gene flow among the sampled populations, there are clear distinctions between populations from the northern desert region and those from the temperate, savannah region. We identified several genes showing population genetic patterns consistent with positive selection within African bee populations, and between these populations and European A. mellifera or Asian Apis florea. CONCLUSIONS: These results lay the groundwork for future studies of adaptive ecological evolution in honey bees, and demonstrate the use of new, freely available web-based tools and workflows ( http://usegalaxy.org/r/kenyanbee ) that can be applied to any model system with genomic information.

Hydroxylation patterns associated with pheromone synthesis and composition in two honey bee subspecies Apis mellifera scutellata and A. m. capensis laying workers.

Colony losses due to social parasitism in the form of reproductive workers of the Apis mellifera capensis clones results from the production of queen-like pheromonal signals coupled with ovarian activation in these socially parasitic honey bees. While the behavioral attributes of these social parasites have been described, their genetic attributes require more detailed exploration. Here, we investigate the production of mandibular gland pheromones in queenless workers of two sub-species of African honey bees; A. m. scutellata (low reproductive potential) and A. m. capensis clones (high reproductive potential). We used standard techniques in gas chromatography to assess the amounts of various pheromone components present, and qPCR to assess the expression of cytochrome P450 genes cyp6bd1 and cyp6as8, thought to be involved in the caste-dependent hydroxylation of acylated stearic acid in queens and workers, respectively. We found that, for both subspecies, the quality and quantity of the individual pheromone components vary with age, and that from the onset, A. m. capensis parasites make use of gene pathways typically upregulated in queens in achieving reproductive dominance. Due to the high production of 9-hydroxy-decenoic acid (9-HDA) the precursor to the queen substance 9-oxo-decenoic acid (9-ODA) in newly emerged capensis clones, we argue that clones are primed for parasitism upon emergence and develop into fully fledged parasites depending on the colony's social environment.

Reproductive parasitism by worker honey bees suppressed by queens through regulation of worker mandibular secretions.

Social cohesion in social insect colonies can be achieved through the use of chemical signals whose production is caste-specific and regulated by social contexts. In honey bees, queen mandibular gland pheromones (QMP) maintain reproductive dominance by inhibiting ovary activation and production of queen-like mandibular gland signals in workers. We investigated whether honey bee queens can control reproductively active workers of the intraspecific social parasite Apis mellifera capensis, parasitising A. m. scutellata host colonies. Our results show that the queen's QMP suppresses ovarian activation and inhibits the production of QMP pheromone signals by the parasitic workers, achieved through differential expression of enzymes involved in the biosynthesis of these pheromones at two points in the biosynthetic pathway. This is the first report showing that honey bee queens can regulate reproduction in intraspecific social parasites and deepens our understanding of the molecular mechanisms involved in the regulation of worker reproduction in social insects.

Evaluation of the distribution and impacts of parasites, pathogens, and pesticides on honey bee (Apis mellifera) populations in East Africa.

In East Africa, honey bees (Apis mellifera) provide critical pollination services and income for small-holder farmers and rural families. While honey bee populations in North America and Europe are in decline, little is known about the status of honey bee populations in Africa. We initiated a nationwide survey encompassing 24 locations across Kenya in 2010 to evaluate the numbers and sizes of honey bee colonies, assess the presence of parasites (Varroa mites and Nosema microsporidia) and viruses, identify and quantify pesticide contaminants in hives, and assay for levels of hygienic behavior. Varroa mites were present throughout Kenya, except in the remote north. Levels of Varroa were positively correlated with elevation, suggesting that environmental factors may play a role in honey bee host-parasite interactions. Levels of Varroa were negatively correlated with levels of hygienic behavior: however, while Varroa infestation dramatically reduces honey bee colony survival in the US and Europe, in Kenya Varroa presence alone does not appear to impact colony size. Nosema apis was found at three sites along the coast and one interior site. Only a small number of pesticides at low concentrations were found. Of the seven common US/European honey bee viruses, only three were identified but, like Varroa, were absent from northern Kenya. The number of viruses present was positively correlated with Varroa levels, but was not correlated with colony size or hygienic behavior. Our results suggest that Varroa, the three viruses, and Nosema have been relatively recently introduced into Kenya, but these factors do not yet appear to be impacting Kenyan bee populations. Thus chemical control for Varroa and Nosema are not necessary for Kenyan bees at this time. This study provides baseline data for future analyses of the possible mechanisms underlying resistance to and the long-term impacts of these factors on African bee populations.