Mechanisms Regulating Swarming Behavior in Honey Bees (Apis Spp.) Christina Grozinger, Jessica Richards, Heather Mattila

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Mechanisms Regulating Swarming Behavior in Honey Bees (Apis Spp.) Christina Grozinger, Jessica Richards, Heather Mattila From molecules to societies: mechanisms regulating swarming behavior in honey bees (Apis spp.) Christina Grozinger, Jessica Richards, Heather Mattila To cite this version: Christina Grozinger, Jessica Richards, Heather Mattila. From molecules to societies: mechanisms regulating swarming behavior in honey bees (Apis spp.). Apidologie, Springer Verlag, 2014, 45 (3), pp.327-346. 10.1007/s13592-013-0253-2. hal-01234732 HAL Id: hal-01234732 https://hal.archives-ouvertes.fr/hal-01234732 Submitted on 27 Nov 2015 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie (2014) 45:327–346 Review article * INRA, DIB and Springer-Verlag France, 2013 DOI: 10.1007/s13592-013-0253-2 From molecules to societies: mechanisms regulating swarming behavior in honey bees (Apis spp.) 1 1 2 Christina M. GROZINGER , Jessica RICHARDS , Heather R. MATTILA 1Department of Entomology, Center for Pollinator Research, The Pennsylvania State University, 4A Chemical Ecology Lab, Orchard Road, University Park, PA 16802, USA 2Department of Biological Sciences, Wellesley College, 106 Central Street, Wellesley, MA 02481, USA Received 16 July 2013 – Revised 18 October 2013 – Accepted 25 October 2013 Abstract – Reproduction by colony fission, or swarming, is a spectacular example of a behavior that requires the simultaneous coordination of the activities of thousands of honey bee workers and their queen. The successful execution of this collective phenomenon relies on the appropriate response of individuals in swarms to a myriad of signals that are produced by workers and queens to synchronize their nest exodus, subsequent house hunting, and eventual relocation to a new nest site. In this review, we describe our current understanding of the social factors that trigger swarming in colonies and the nonchemical and chemical signals that mediate a coordinated transition between its stages. We also highlight emerging work on the physiological and genomic mechanisms underpinning swarming behavior. Finally, we discuss the possible evolutionary origins of swarming behavior, through comparisons with related behaviors of migration, overwintering, estivation, and diapause in honey bees and other insects. collective behavior / swarming / chemical communication / physiology / genomics / honey bee 1. INTRODUCTION involved interactions between a small number of individuals (i.e., courtship, mating, and aggres- Elucidating the proximate and ultimate mech- sion; Clayton 2004; Villella and Hall 2008; anisms that regulate social behavior is one of the Anholt and Mackay 2012; Cummings 2012)or, great challenges in biology. With the development in the case of social insects, differences between of new genomic tools and resources, it is individuals who specialize in different tasks becoming increasingly feasible to examine these within a group (e.g., division of labor, Smith et questions in a wide array of species in their natural al. 2008). The molecular mechanisms that regu- habitats and to perform sophisticated comparative late collective behaviors, in which the majority of studies that examine the molecular mechanisms individuals in a group perform a coordinated by which social behavior evolved from solitary behavior, have not been comprehensively exam- behaviors (reviewed in Toth and Robinson 2007; ined outside of aggregations of single-celled Robinson et al. 2008). However, the majority of organisms such as bacteria, yeast, and social social behaviors that have been studied have amoeba (Velicer and Yu 2003; Queller 2008;Li and Purugganan 2011), with the exception of gregarious behavior in migrating locusts (Ma et al. 2011; Ott et al. 2012). Examples of such collective Corresponding author: C. M. Grozinger, behaviors include schooling in fish, migration in [email protected] birds or locusts, and synchronized applause in Manuscript editor: Stan Schneider human audiences (Sumpter 2006), where a group 328 C.M. Grozinger et al. of individuals, regardless of their individual states mechanisms regulating swarming behavior have or preferences, simultaneously perform similar only recently been considered (Liang et al. behaviors such that the group behaves cohesively. 2012; Richards et al. unpublished data). In a honey bee colony, there are several Swarming requires communication and coordi- colony-level phenomena in which the behavior nation on a grand scale, making it an excellent of a queen and tens of thousands of her worker model system in which to examine the social daughters must be coordinated to sustain their and molecular mechanisms that organize this colony's survival and function. In established collective behavior in an effort to understand colonies, one of these phenomena is reproduc- how such complex processes could evolve. tive division of labor, where queens lay eggs While there has been considerable interest in that are tended to adulthood by facultatively elucidating the behavioral and chemical signals sterile workers, who typically lay eggs only in that coordinate swarming, how these are the absence of a queen and brood (Wilson translated at the genomic and physiological 1971). Workers also exhibit age-based division level into changes in behavior remain largely of labor, where they specialize on different tasks uncharacterized. Here, we will review the factors as they mature, with young “nurse” bees that stimulate a colony to prepare to swarm, the performing brood care and older “forager” bees nonchemical and chemical signals that coordinate collecting resources from the environment the swarm's departure and movement to a new (Robinson 1992; Seeley 1995). Foraging itself nest site, and the genomic and physiological is another essential colony-level process where pathways that are associated with a worker's the activities of a substantial portion of the decision to depart with the swarm or remain in population are finely coordinated to facilitate the colony. We will also explore the possible efficient discovery and exploitation of profitable evolutionary origins of swarming behavior in food sources (reviewed in Seeley 1995). A final honey bees, comparing and contrasting swarming and remarkable example is that of reproductive with diapause in solitary insects, overwintering swarming (hereafter referred to simply as and estivation in honey bees and migration in “swarming”), a process of colony fission in tropical honey bees, and highlight research ques- which a colony's queen and approximately two- tions that may provide insights into the evolution thirds to three-quarters of its workers leave their of this fascinating behavior. original (or parental) nest to find a new colony (Martin 1963; Getz et al. 1982; Rangel and Seeley 2012). Upon leaving, a swarm's workers 2. OVERVIEW OF SWARM form a temporary cluster (called a bivouac) and PREPARATION AND SWARMING initiate a search for a new nest site while they IN HONEY BEE COLONIES are homeless. The workers who remain behind raise one of the queen's daughters as their new Swarming is a complex, multi-step process queen (reviewed in Winston 1987;Seeley that is mediated by multiple environmental, 2010). social, physiological, and molecular factors Previous studies have examined the molecu- (see Figure 1). Swarming typically occurs lar mechanisms that regulate reproductive divi- during specific times of the year, usually when sion or labor, worker division of labor, and resources are plentiful to support rapid popula- foraging in honey bees (Whitfield et al. 2006b; tion growth (Simpson 1959). This population Grozinger et al. 2007a; Page et al. 2012), and growth underpins four colony-level changes that the information gained from these studies has have been hypothesized to trigger swarming laid the groundwork to examine how these preparation: increasing colony size (in terms of complex social behaviors evolved from behav- both number of workers and amount of comb), iors observed in solitary species (i.e., Ben- congestion of the brood nest, skewing of worker Shahar et al. 2002). However, the molecular age distribution toward younger individuals, Mechanisms regulating swarming 329 Figure 1. Overview of swarming in honey bees, A. mellifera. Reproductive swarming in honey bees occurs via a series of distinct phases (shown in orange and depicted graphically). The activities of colony members during these phases and their transitions are coordinated by nonchemical (highlighted in black) and chemical signals (highlighted in yellow) from queens and workers. In cases where signals coordinate swarm movement (i.e., exodus or liftoff), we note the period of time prior to movement during which the signals are produced. We hypothesize that volatile queen pheromones are involved in swarm exodus and liftoff (designated as “possible queen pheromone”), but further studies are necessary to confirm this. Finally, note that “rapid population growth” prior to swarming leads to other colony conditions that may trigger swarm preparation, including increased colony size and congestion, congestion of the brood nest, and decreased concentration and/or transmission
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