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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Available from: Terry Burke, Aug 08, 2015
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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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    ABSTRACT: Ovarian activity not only influences fertility, but is also involved with the regulation of division of labour between reproductive and behavioural castes of female honey bees. In order to identify candidate genes associated with ovarian activity, we compared the gene expression patterns between inactivated and activated ovaries of queens and workers by means of high-throughput RNA-sequencing technology. A total of 1615 differentially expressed genes (DEGs) was detected between ovaries of virgin and mated queens, and more than 5300 DEGs were detected between inactivated and activated worker ovaries. Intersection analysis of DEGs amongst five libraries revealed that a similar set of genes (824) participated in the ovary activation of both queens and workers. A large number of these DEGs were predominantly related to cellular, cell and cell part, binding, biological regulation and metabolic processes. In addition, over 1000 DEGs were linked to more than 230 components of Kyoto Encyclopedia of Genes and Genomes pathways, including 25 signalling pathways. The reliability of the RNA-sequencing results was confirmed by means of quantitative real-time PCR. Our results provide new insights into the molecular mechanisms involved in ovary activation and reproductive division of labour.
    Insect Molecular Biology 08/2014; 23(5). DOI:10.1111/imb.12114 · 2.98 Impact Factor
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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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    ABSTRACT: Kin selection theory predicts that honeybee (Apis mellifera) workers should largely refrain from producing their own offspring, as the workers collectively have higher inclusive fitness if they rear the sons of their mother, the queen. Studies that have quantified levels of ovary activation and reproduction among workers have largely supported this prediction. We sampled pre-emergent male pupae and adult workers from seven colonies at regular intervals throughout the reproductive part of the season. We show that the overall contribution of workers to male (drone) production is 4.2%, nearly 40 times higher than is generally reported, and is highest during reproductive swarming, when an average of 6.2% of the males genotyped are worker-produced. Similarly, workers in our samples were 100 times more likely to have active ovaries than previously assumed. Worker reproduction is seasonally influenced and peaks when colonies are rearing new queens. Not all worker subfamilies contribute equally to reproduction. Instead, certain subfamilies are massively over-represented in drone brood. By laying eggs within the period in which many colonies produce virgin queens, these rare worker subfamilies increase their direct fitness via their well-timed sons.
    Molecular Ecology 07/2013; 22(16). DOI:10.1111/mec.12387 · 5.84 Impact Factor
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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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    ABSTRACT: A conspicuous feature of honey bee social bio-logy is the division of labour between reproductive queens and functionally sterile workers. However, the sterility of workers is conditional and sensitive to genetic and envi-ronmental context. Despite this understanding, we do not yet know how effective differences in genotype versus differ-ences in colony environment are for generating variation in levels of ovary activation in a population of workers. We therefore performed a field study and meta-analysis to esti-mate the standardized effect size g of broad 'environmental' and 'genetic' manipulations on worker ovary scores. Despite considerable differences in methodology and treatment among published studies, we report that both genetic and environmental manipulations were effective at generating differences in ovary phenotype between groups of worker bees. Our analysis found that environmental treatments, such as differences in pheromones and diet, had a larger mean effect on worker ovary activation scores than have genetic factors such as patriline or strain (g = 0.54 vs. 0.39). We conclude by discussing the biological significance of envi-ronmentally sensitive sterility in honey bee societies.
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