Thelytoky in the honey bee

Abstract

Thelytoky, the asexual production of females, is rare in honey bees. However, it is ubiquitous in workers of the Cape honey bee Apis mellifera capensis. Thelytoky allows some workers to be reincarnated into the queen phenotype, and thereby selects for reproductive competition among workers. Thelytoky also acts as an exaptation for the emergence of reproductive parasites, the most extreme example of which is an entirely clonal 'cancerous' lineage of workers (the Clone) that lethally parasitises colonies of another subspecies Apis mellifera scutellata. The Clone is an enigma because thelytoky results in the accumulation of homozygosity at any loci that are free to recombine, yet the Clone retains considerable heterozygosity. The Clone pays a cost for its thelytoky: the selective removal of homozygous offspring at each generation. We propose that workers, queens and Clones have differing abilities to endure the costs and benefits of sex and asexuality, accounting for the heterogeneous distribution of reproductive strategies across the A. mellifera capensis population. We further suggest that multiple factors must fall into place for thelytoky to emerge as an effective reproductive strategy in a honey bee population, and that geographic isolation resulting in genetic drift and founder effects may have enabled thelytoky to emerge in A. mellifera capensis. Finally, we consider the honey bee in the broader context of haplodiploid Hymenoptera, and argue that constraints on the evolution of sex in non-haplodiploid taxa may make sexual reproduction an evolutionary 'one-way street'.

Genetic reincarnation of workers as queens in the Eastern honeybee Apis cerana

“…When workers reproduce thelytokously, they are related to their own daughters by unity and are therefore far less likely to refrain from personal reproduction (Greeff, 1996). More importantly, thelytoky opens the possibility for workers to be reincarnated as queens if their daughter is raised as the next queen (Jordan et al, 2008;Goudie and Oldroyd, 2014). We therefore expect workers to compete strongly with their sisters, resulting in high levels of ovary activation (Greeff, 1996).…”

“…), thelytoky is ubiquitous only in a subspecies of Apis mellifera, the Cape honeybee A. m. capensis (Rabeling and Kronauer, 2013). Thelytoky is either absent or very rare in all other honeybees (Mackensen, 1943;Goudie and Oldroyd, 2014). This absence is quite surprising because a worker that reproduces thelytokously has the potential to enormously raise her personal fitness by laying an egg in a queen cell.…”

“…In honeybees, queens and workers are genetically identical and caste differentiation is triggered by differential feeding of very young larvae (de Wilde and Beetsma, 1982;Kucharski et al, 2008), so any diploid egg laid in a queen cell can develop into a queen. A thelytokous worker can therefore be genetically reincarnated as a queen if she lays her egg in a queen cell (Goudie and Oldroyd, 2014). Thelytoky has selected for highly competitive workers in A. m. capensis (reviewed in ; workers in colonies with a queen typically have much higher rates of ovary activation than other (sub)species, and workers specifically target queen cells for oviposition (reviewed in Goudie and Oldroyd, 2014).…”

“…A thelytokous worker can therefore be genetically reincarnated as a queen if she lays her egg in a queen cell (Goudie and Oldroyd, 2014). Thelytoky has selected for highly competitive workers in A. m. capensis (reviewed in ; workers in colonies with a queen typically have much higher rates of ovary activation than other (sub)species, and workers specifically target queen cells for oviposition (reviewed in Goudie and Oldroyd, 2014).…”

“…When virgin queens of commercial strains of A. mellifera are induced to lay under CO 2 narcosis, B1% of the eggs they produce develop into females (Mackensen, 1943). Although this may be the result of developmental errors during arrhenotoky (the process by which a haploid egg develops into a male) (Goudie and Oldroyd, 2014), it is suggestive that thelytoky is a rare or perhaps latent trait in honeybees that appears and is selected for under certain environmental conditions.…”