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Anarchy in the UK: Detailed genetic analysis of worker reproduction in a naturally occurring British anarchistic honeybee, Apis mellifera, colony using DNA microsatellites

Laboratory of Apiculture & Social Insects, Sheffield Molecular Genetics Facility, Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield S10 2TN, UK.
Molecular Ecology (Impact Factor: 5.84). 10/2002; 11(9):1795-803. DOI: 10.1046/j.1365-294X.2000.01569.x
Source: PubMed

ABSTRACT Anarchistic behaviour is a very rare phenotype of honeybee colonies. In an anarchistic colony, many workers' sons are reared in the presence of the queen. Anarchy has previously been described in only two Australian colonies. Here we report on a first detailed genetic analysis of a British anarchistic colony. Male pupae were present in great abundance above the queen excluder, which was clearly indicative of extensive worker reproduction and is the hallmark of anarchy. Seventeen microsatellite loci were used to analyse these male pupae, allowing us to address whether all the males were indeed workers' sons, and how many worker patrilines and individual workers produced them. In the sample, 95 of 96 of the males were definitely workers' sons. Given that approximately 1% of workers' sons were genetically indistinguishable from queen's sons, this suggests that workers do not move any queen-laid eggs between the part of the colony where the queen is present to the area above the queen excluder which the queen cannot enter. The colony had 16 patrilines, with an effective number of patrilines of 9.85. The 75 males that could be assigned with certainty to a patriline came from 7 patrilines, with an effective number of 4.21. They were the offspring of at least 19 workers. This is in contrast to the two previously studied Australian naturally occurring anarchist colonies, in which most of the workers' sons were offspring of one patriline. The high number of patrilines producing males leads to a low mean relatedness between laying workers and males of the colony. We discuss the importance of studying such colonies in the understanding of worker policing and its evolution.

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    • "Variation in worker reproductive traits also occurs in populations of European honey bees although it is restricted to the production of haploid males. These variations have a genetically inherited component as strains with different ovarian activity have been selected from wild-type populations (Barron & Oldroyd, 2001; Châline et al., 2002; Holmes et al., 2013). An extreme example is the mutant strain of 'anarchistic' bees where workers are reproductively active even in the presence of the queen (Oldroyd et al., 1994; Thompson et al., 2006; Oldroyd & Beekman, 2008). "
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    • "This strongly indicates that worker reproduction is more common than previously thought (Page & Erickson 1988; Visscher 1989), but only during the period of reproductive swarming. Nonetheless, in none of our colonies were the majority of drones worker-laid, as observed in previous studies (Oldroyd et al. 1994; Montague & Oldroyd 1998; Chaline et al. 2002). This suggests that the colony studied by Montague and Oldroyd (Montague & Oldroyd 1998), which subsequently gave rise to the selected anarchistic line maintained at Sydney University (Oldroyd & Osborne 1999; Beekman & Oldroyd 2008), was exceptional. "
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    • "Presumably, the patriline effect evident within these colonies is indicative of paternal genes that are responsive to social circumstance and that influence ovary activation (Oldroyd and Thompson, 2007). Anarchic bees highlight the role of genotype in the conditional expression of sterility; not only do anarchic (egg-laying) workers belong to particular patrilines within individual colonies (Châline et al., 2002; Montague and Oldroyd, 1998; Oldroyd et al., 1994) but they also respond to artificial selection, indicating significant additive genetic variation for egg-laying behaviour (Oldroyd and Osborne, 1999; Oxley et al., 2008). In effect, the anarchic lines reveal additive genetic variation for sterility, similar to other honey bee strains with heritable variation for worker reproduction (Hunt et al., 2007; Diniz et al., 1993; Ruttner and Hesse, 1981; Thuller et al., 1996). "
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