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: 6.49). 10/2002; 11(9):1795-803. DOI: 10.1046/j.1365-294X.2000.01569.x
Source: PubMed


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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    • "Therefore, AWs just have to synthesize the final compound 9-ODA by oxidization of 9-HDA, to shift from a workerlike mandibular gland signal to a queen-like signal (Hepburn and Allsopp 1994) dominated by 9- ODA, which allows them to rapidly dominate reproduction (Ruttner and Hesse 1981; Zheng et al. 2010). Our results confirmed anarchistic syndrome occurred in three A. mellifera queenright colonies of European subspecies origin sampled in China, which is observed only in the four other countries before, New Zealand, Australia, America, and the UK under natural conditions (Oldroyd et al. 1994; Ratnieks 1995; Montague and Oldroyd 1998; Châline et al. 2002 "
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    ABSTRACT: In honey bee colonies, workers, in particular of " anarchistic " lineages, can activate their ovaries and lay eggs, even in the presence of the queen. We identified three queenright colonies showing typical signs of worker reproduction. To characterize this new lineage, we extracted the mandibular gland and analyzed it using gas chromatography. The total amounts of the five main components of the mandibular gland, namely methyl p-hydroxyben-zoate (HOB), 9-oxo-2(E)-decenoic acid (9-ODA), (S)-9-hydroxy-(E)-2-decenoic acid (9-HDA), 10-HDA, and 10-hydroxyde-canoic acid (10-HDAA) were significantly higher in the mandibular gland profiles of workers with activated ovaries (AWs, 8.88±1.71 μg) compared to workers with inactivated ovaries (IAWs, 4.00± 2.09 μg). Furthermore, the chemical profiles of IAWs were dominated by the " worker substances " 10-HDA (34.64± 8.19 %) and its precursor 10-HDAA (22.88±4.95 %), while the chemical profiles in AWs were dominated by the precursor of the queen substance 9-HDA (40.04±7.55 %). The ratios of two precursor substances 10-HDAA/9-HDA of IAWs were more worker like (>1.0) whereas AWs were more queen like (≤1.0). These results suggest that the mandibular pheromones of anarchistic workers resemble a more queen-like reproductive active profile and that these workers may represent a reversion to a more basal reproductive phenotype. Apis mellifera / anarchistic colony / ovary activation / egg production / worker policing / worker mandibular gland pheromone
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    • "Nevertheless, colonies are sometimes found in which the normally infertile workers activate their ovaries and lay eggs even when a queen is present (Oldroyd et al. 1994; Montague and Oldroyd 1998; Châline et al. 2002). Studies of these 'anarchistic' workers have established that ovary activation has a strong genetic basis (Oldroyd et al. 1994; Montague and Oldroyd 1998; Châline et al. 2002; Thompson et al. 2006). "
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    ABSTRACT: Worker sterility is a defining characteristic of eusociality. The existence of the sterileworker caste remains a fundamental question for evolutionary biology as it requires the existence of genes that reduce personal reproduction. Currently, little is known about the proximate mechanisms underpinning worker sterility. Studies into a mutant “anarchistic” strain (in which workers can activate their ovaries) of honey bee, Apis mellifera, identified a list of candidate genes that regulate ovary activation.Wequantified the expression of the fourmost promising candidate genes (Anarchy, Pdk1, S6k,and Ulk3) in nonactivated and activated ovaries of wild-type workers. Ovarian expression of Anarchy, a peroxisomal membrane protein, predicts the ovary state of workers with 88.2%accuracy. Increased expression of Anarchy in the ovary is strongly associated with suppression of oogenesis and its expression is sensitive to the presence of the queen. Therefore, Anarchy satisfies key criteria for a “gene underlying altruism”.When we knockeddownexpressionof Anarchy in the ovary using RNA interference (RNAi) we altered the expression of Buffy, a gene that regulates programmed cell death.Whole-mount multiplex fluorescent in situ hybridization (mFISH) shows Anarchy transcripts localize to degenerating oocytes within the ovary. Our results suggest that Anarchy is involved in the regulation of oogenesis through programmed cell death. The evolution of facultative worker sterility most likely occurred when the conserved mechanism of programmed cell death was co-opted to regulate ovary activation. Anarchy may therefore be the first example of a gene that has evolved through kin selection to regulate worker sterility.
    No preview · Article · Jan 2016 · Molecular Biology and Evolution
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    • "This capacity for virgin birth provides workers with an (albeit limited ) opportunity for direct reproduction after they have lost their queen (reviewed in Beekman and Oldroyd, 2008; Winston, 1987). Furthermore, whenever circumstances arise where workers can benefit from personal reproduction over indirect reproduction via their queen, workers can activate their ovaries to reproductively parasitize their own or other colonies (Châline et al., 2002; Chapman et al., 2009a,b, 2010; Lopez-Vaamonde et al., 2004; Nanork et al., 2007, 2005; Oldroyd et al., 1994; Takahashi et al., 2010). "
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    ABSTRACT: If a honey bee (Apis spp.) colony becomes queenless, about 1/3 of young workers activate their ovaries and produce haploid male-producing eggs. In doing so queenless workers maximize their inclusive fitness because the normal option of vicarious production of relatives via their queen's eggs is no longer available. But if many workers are engaged in reproduction, how does a queenless colony continue to feed its brood and forage? Here we show that in the Asian hive bee Apis cerana hypopharyngeal (HPG) size is larger in queenless workers than in queenright workers and that bees undertaking brood-rearing tasks have larger HPG than same-aged bees that are foraging. In queenless colonies, workers with a smaller number of ovarioles are more likely to have activated ovaries. This reinforces the puzzling observation that a large number of ovarioles reduces reproductive success in queenless A. cerana. It further suggests that reproductive workers either avoid foraging or transition to foraging later in life than non-reproductive workers. Finally, our study also showed that ovary activation and larger-than-average numbers of ovarioles had no statistically detectable influence on foraging specialization for pollen or nectar. Copyright © 2015. Published by Elsevier Ltd.
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