Academic journal article Genetics

Thelytokous Parthenogenesis in Unmated Queen Honeybees (Apis Mellifera Capensis): Central Fusion and High Recombination Rates

Academic journal article Genetics

Thelytokous Parthenogenesis in Unmated Queen Honeybees (Apis Mellifera Capensis): Central Fusion and High Recombination Rates

Article excerpt

ABSTRACT

The subspecies of honeybee indigenous to the Cape region of South Africa, Apis mellifera capensis, is unique because a high proportion of unmated workers can lay eggs that develop into females via thelytokous parthenogenesis involving central fusion of meiotic products. This ability allows pseudoclonal lineages of workers to establish, which are presently widespread as reproductive parasites within the honeybee populations of South Africa. Successful long-term propagation of a parthenogen requires the maintenance of heterozygosity at the sex locus, which in honeybees must be heterozygous for the expression of female traits. Thus, in successful lineages of parasitic workers, recombination events are reduced by an order of magnitude relative to meiosis in queens of other honeybee subspecies. Here we show that in unmated A. m. capensis queens treated to induce oviposition, no such reduction in recombination occurs, indicating that thelytoky and reduced recombination are not controlled by the same gene. Our virgin queens were able to lay both arrhenotokous male-producing haploid eggs and thelytokous female-producing diploid eggs at the same time, with evidence that they have some voluntary control over which kind of egg was laid. If so, they are able to influence the kind of second-division meiosis that occurs in their eggs post partum.

IN the honeybee, Apis mellifera, unfertilized eggs normally develop into haploid males by arrhenotokous parthenogenesis. Unfertilized eggs are produced by queens for the production of males and also by unmated queenless workers whose eggs also produce functional males (Dzierzon 1845). Very occasionally, however, a worker will lay an egg in which meiosis II is modified so that an unfertilized egg is able to restore diploidy and become female (Mackensen 1943; Tucker 1958), in a form of parthenogenesis known as thelytoky. Thelytoky is ubiquitous in workers of the South African subspecies A. m. capensis (hereafter Cape) (Onions 1912; Anderson 1963) and is thought to be controlled by a single gene, Th, which a mapping study has suggested may be homologous to Grainy Head of Drosophila melanogaster (Lattorff et al. 2005, 2007). In Cape workers, two haploid pronuclei of second-division meiosis fuse and produce a diploid zygote, which usually gives rise to a female that may be reared as a worker or a queen (Moritz et al. 1996; Jordan et al. 2008). Some Cape workers use this ability to produce female offspring and reproductively parasitize other colonies (Allsopp 1993; Neumann et al. 2001; Baudry et al. 2004; Dietemann et al. 2006; Jordan et al. 2008).

During this form of automictic (meiotic) thelytokous parthenogenesis there is a normal reduction division, bivalent formation and formation of chiasmata during meiosis I (Verma and Ruttner 1983). If a locus is distant from the centromere there will be multiple recombination events between the locus and the centromere, and the two pairs of alleles will become randomly placed on the four chromatids. Thus thelytokous parthenogenesis involving recombination means that for any locus heterozygous in the mother, there is a one of three chance that the offspring will be homozygous, whichever way the pronuclei combine (Table 1; Pearcy et al. 2006). This ratio arises because if we choose any one chromatid at random, two of the three remaining chromatids will carry the alternate allele.

If there is interference to recombination or if loci are positioned close to the centromere and cannot recombine, the way in which the chromatids fuse determines what happens to the zygosity of offspring. During thelytokous parthenogenesis the products of meiosis II can fuse in one of three ways (Suomalainen et al. 1987; Pearcy et al. 2006). Let us assume that the four haploid pronuclei of meiosis II are aligned in a row as in A1A2B1B2. A1 and A2 were derived from nucleus A of meiosis I and B1 and B2 were derived from nucleus B. Under terminal fusion, terminal pronuclei fuse (i. …

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