Article

Royalactin induces queen differentiation in honeybees. Biotechnology Research Center. Nature

Biotechnology Research Center, Toyama Prefectural University, Imizu, Toyama 939-0398, Japan.
Nature (Impact Factor: 41.46). 05/2011; 473(7348):478-83. DOI: 10.1038/nature10093
Source: PubMed

ABSTRACT

The honeybee (Apis mellifera) forms two female castes: the queen and the worker. This dimorphism depends not on genetic differences, but on ingestion of royal jelly, although the mechanism through which royal jelly regulates caste differentiation has long remained unknown. Here I show that a 57-kDa protein in royal jelly, previously designated as royalactin, induces the differentiation of honeybee larvae into queens. Royalactin increased body size and ovary development and shortened developmental time in honeybees. Surprisingly, it also showed similar effects in the fruitfly (Drosophila melanogaster). Mechanistic studies revealed that royalactin activated p70 S6 kinase, which was responsible for the increase of body size, increased the activity of mitogen-activated protein kinase, which was involved in the decreased developmental time, and increased the titre of juvenile hormone, an essential hormone for ovary development. Knockdown of epidermal growth factor receptor (Egfr) expression in the fat body of honeybees and fruitflies resulted in a defect of all phenotypes induced by royalactin, showing that Egfr mediates these actions. These findings indicate that a specific factor in royal jelly, royalactin, drives queen development through an Egfr-mediated signalling pathway.

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    • "These studies demonstrate that the caste developmental programme includes nurse worker genes with IGEs on caste, so that focusing solely on direct genetic effects expressed in developing larvae yields an incomplete picture of the genetic basis of caste. Some of the putative honey bee genes with IGEs on caste have been identified, including two major royal jelly protein genes (Huang et al., 2012; Kamakura, 2011), and hundreds of additional genes with putative IGEs on caste have recently been identified through RNA sequencing of the heads and royal jelly producing glands of nurse bees feeding queen-versus workerdestined larvae (Vojvodic et al., 2014). These nurse worker genes presumably affect larval development by affecting the quality and quantity of provisioned food as well as by affecting the provisioning behaviour of nurse workers. "
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    ABSTRACT: The social complexity that characterizes the eusocial insects strongly affects all aspects of social insect life, including the molecular and evolutionary genetic basis of social insect traits. Quantitative genetic theory and empirical approaches have been developed over the past 60 years specifically to study the genetic implications of social interactions. Surprisingly, given the obvious biological importance of social interactions in social insects, this research tradition has been and continues to be widely overlooked throughout the social insect literature, including in recent sociogenomic studies focused on understanding the molecular underpinnings of social life. Instead, the overwhelming majority of social insect genetic research has relied on conventional genetic approaches developed for solitary organisms focused on the one-to-one association of an individual's genes to its own traits. I survey social insect studies that conclusively demonstrate the importance of indirect genetic effects (IGEs), which arise from social interactions, for social insect trait expression and evolution. I explain why these genetically based social effects are expected to be ubiquitous in social insects and I explain the relevance of the IGE framework, originally developed within quantitative genetics, for molecular genetic studies of social insect traits such as behaviour and caste. I discuss the problems of ignoring IGEs and relying solely on conventional direct genetic effect approaches. Finally, I discuss the strong potential of using the IGE approach and other more systems-level-focused approaches to complement conventional reductionist approaches in elucidating the genetic basis of social insect trait expression and evolution.
    Full-text · Article · Dec 2015 · Advances in insect physiology
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    • "Most of the genes found in the honey bee genome were shared with solitary animals, and there were no obvious genomic features underlying social evolution in the enigmatic honey bee. The reference genome did however revolutionize research on the molecular basis of caste phenotypes by illuminating the relationships between physiology, transcription, methylation, behaviour and caste differences in honey bees (Hunt et al., 2007; Kamakura, 2011; Kucharski et al., 2008; Lyko et al., 2010; Robinson et al., 2008; Zayed and Robinson, 2012) (the chapter 'Insect Reward Systems: Comparing Flies and Bees' by Søvik et al.; the chapter 'Old Threads Make New Tapestry—Rewiring of Signalling Pathways Underlies Caste Phenotypic Plasticity in the Honey Bee, Apis mellifera L.' by Hartfleder et al.). The mechanistic studies vastly increased our knowledge of 'social life in molecular terms' (Robinson et al., 2005) but provided little insight into the process of social evolution. "
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    ABSTRACT: Genomics revolutionized the field of social insect research by providing powerful tools to understand the relationship between genes, physiology and behaviour of social insects. Notably, analysis of gene expression and methylation patterns in the different castes of insect colonies highlighted many genes that likely underlie caste-specific physiological and behavioural phenotypes. However, earlier studies of social insect genomes lacked an ‘evolutionary’ context. Out of the millions of DNA bases found in the genome of a social insect, which pieces were most important to fitness over the timescale of social evolution? Here, we review a burgeoning body of literature that utilizes between-species or within-species genomic comparisons to highlight the evolutionary forces that have shaped social insect genomes. These pioneering phylogenetic and population genomic studies provide a critically needed evolutionary context to social insect genomes and underscore the importance of adaptive changes in physiology and behaviour in social evolution.
    Full-text · Article · Dec 2015 · Advances in insect physiology
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    • "In many species, a eusocial colony is composed of one queen and largely non-reproductive workers that are the queen's offspring (Wilson, 1971, Michener, 1974). Whether a queen's offspring becomes a worker or a future queen is often mediated by the queen herself: for example, (1) the queen in some social wasps and bees maintains the reproductive monopoly of the colony through aggression (Fletcher and Ross, 1985); (2) in many social insects the queen can feed offspring with food of different quantity or quality influencing offspring's future reproductive caste (i.e., queen or worker) (e.g., O'Donnell, 1998, Bourke and Ratnieks, 1999, Kapheim et al., 2011, Brand and Chapuisat, 2012); (3) in an ant species the queen can deposit hormones in the eggs inducing offspring to develop into workers (Schwander et al., 2008); (4) in certain wasp and termite species the queen can produce pheromones that prevent offspring from becoming queens (Bhadra et al., 2010, Matsuura et al., 2010); and (5) in honeybees queen pheromones can induce workers to feed larvae without royal jelly causing larvae to develop into workers (Le Conte and Hefetz, 2008, Kamakura, 2011). In addition to influencing caste determination, queens can use pheromones to keep workers' ovaries undeveloped (e.g., Holman et al., 2010, Van Oystaeyen et al., 2014), and to alter workers' brain functioning inducing workers to perform various tasks (Beggs et al., 2007). "
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    ABSTRACT: In many eusocial species, queens use pheromones to influence offspring to express worker phenotypes. Although evidence suggests that queen pheromones are honest signals of the queen's reproductive health, here I show that queen's honest signalling can result from ancestral maternal manipulation. I develop a mathematical model to study the coevolution of maternal manipulation, offspring resistance to manipulation and maternal resource allocation. I assume that (i) maternal manipulation causes offspring to be workers against offspring's interests; (ii) offspring can resist at no direct cost, as is thought to be the case with pheromonal manipulation; and (iii) the mother chooses how much resource to allocate to fertility and maternal care. In the coevolution of these traits, I find that maternal care decreases, thereby increasing the benefit that offspring obtain from help, which in the long run eliminates selection for resistance. Consequently, ancestral maternal manipulation yields stable eusociality despite costless resistance. Additionally, ancestral manipulation in the long run becomes honest signalling that induces offspring to help. These results indicate that both eusociality and its commonly associated queen honest signalling can be likely to originate from ancestral manipulation.
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