Asexually produced Cape honeybee queens (Apis mellifera capensis) reproduce sexually.

Unmated workers of the Cape honeybee Apis mellifera capensis can produce female offspring including daughter queens. As worker-laid queens are produced asexually, we wondered whether these asexually produced individuals reproduce asexually or sexually. We sampled 11 colonies headed by queens known to be the clonal offspring of workers and genotyped 23 worker offspring from each queen at 5 microsatellite loci. Without exception, asexually produced queens produced female worker offspring sexually. In addition, we report the replacement of a queen by her asexually produced granddaughter, with this asexually produced queen also producing offspring sexually. Hence, once a female larva is raised as a queen, mating and sexual reproduction appears to be obligatory in this subspecies, despite the fact that worker-laid queens are derived from asexual lineages.

Selection on overdominant genes maintains heterozygosity along multiple chromosomes in a clonal lineage of honey bee.

Correlations between fitness and genome-wide heterozygosity (heterozygosity-fitness correlations, HFCs) have been reported across a wide range of taxa. The genetic basis of these correlations is controversial: do they arise from genome-wide inbreeding ("general effects") or the "local effects" of overdominant loci acting in linkage disequilibrium with neutral loci? In an asexual thelytokous lineage of the Cape honey bee (Apis mellifera capensis), the effects of inbreeding have been homogenized across the population, making this an ideal system in which to detect overdominant loci, and to make inferences about the importance of overdominance on HFCs in general. Here we investigate the pattern of zygosity along two chromosomes in 42 workers from the clonal Cape honey bee population. On chromosome III (which contains the sex-locus, a gene that is homozygous-lethal) and chromosome IV we show that the pattern of zygosity is characterized by loss of heterozygosity in short regions followed by the telomeric restoration of heterozygosity. We infer that at least four selectively overdominant genes maintain heterozygosity on chromosome III and three on chromosome IV via local effects acting on neutral markers in linkage disequilibrium. We conclude that heterozygote advantage and local effects may be more common and evolutionarily significant than is generally appreciated.

Maintenance and loss of heterozygosity in a thelytokous lineage of honey bees (Apis mellifera capensis).

An asexual lineage that reproduces by automictic thelytokous parthenogenesis has a problem: rapid loss of heterozygosity resulting in effective inbreeding. Thus, the circumstances under which rare asexual lineages thrive provide insights into the trade-offs that shape the evolution of alternative reproductive strategies across taxa. A socially parasitic lineage of the Cape honey bee, Apis mellifera capensis, provides an example of a thelytokous lineage that has endured for over two decades. It has been proposed that cytological adaptations slow the loss of heterozygosity in this lineage. However, we show that heterozygosity at the complementary sex determining (csd) locus is maintained via selection against homozygous diploid males that arise from recombination. Further, because zygosity is correlated across the genome, it appears that selection against diploid males reduces loss of homozygosity at other loci. Selection against homozygotes at csd results in substantial genetic load, so that if a thelytokous lineage is to endure, unusual ecological circumstances must exist in which asexuality permits such a high degree of fecundity that the genetic load can be tolerated. Without these ecological circumstances, sex will triumph over asexuality. In A. m. capensis, these conditions are provided by the parasitic interaction with its conspecific host, Apis mellifera scutellata.