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Social Immunity and the Superorganism: Behavioral Defenses Protecting Honey Bee Colonies from Pathogens and Parasites

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Social Immunity and the Superorganism: Behavioral Defenses Protecting Honey Bee Colonies from Pathogens and Parasites Bee World ISSN: 0005-772X (Print) 2376-7618 (Online) Journal homepage: http://www.tandfonline.com/loi/tbee20 Social Immunity and the Superorganism: Behavioral Defenses Protecting Honey Bee Colonies from Pathogens and Parasites Michael Simone-Finstrom To cite this article: Michael Simone-Finstrom (2017) Social Immunity and the Superorganism: Behavioral Defenses Protecting Honey Bee Colonies from Pathogens and Parasites, Bee World, 94:1, 21-29, DOI: 10.1080/0005772X.2017.1307800 To link to this article: http://dx.doi.org/10.1080/0005772X.2017.1307800 Published online: 21 Apr 2017. Submit your article to this journal View related articles View Crossmark data Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=tbee20 Download by: [199.133.186.96] Date: 21 April 2017, At: 07:59 REVIEW ARTICLE Social Immunity and the Superorganism: Behavioral Defenses Protecting Honey Bee Colonies from Pathogens and Parasites Michael Simone-Finstrom Introduction the reduced investment in physiological to suffocate the hornet and preventing immunity or as a result of the reliance on colony infestation (Sugahara & Sakamoto, Understanding the complexities of social colony-level defenses relaxing the selec- 2009). insect immunity, that is, how insects tion pressure for a stronger individual combat pathogens, parasites and pests, is immune defense (Harpur & Zayed, 2013). Due to the connections between indi- a fundamental question that not only has vidual, physiological immunity and broad applications for understanding dis- Traits that reduce pathogen and parasite colony-level social immune mechanisms, ease dynamics in social groups (Fefferman infection intensity and transmission at common terminology for how these & Traniello, 2008) (e.g., human societies) the colony level are referred to as “social traits are expressed is also being adopted but also practical benefits for improving immunity” (Cremer, Armitage, & Schmid- (Cremer & Sixt, 2009). These mechanisms honey bee stocks for increased health and Hempel, 2007). Recent iterations have function across a gradient of constitutive productivity. When we first consider the been proposed to expand the definition immune defenses to those that are highly concept of immunity in any organism, of social immunity to apply to not just inducible (Figure 1). Constitutive defenses the tendency is to think at the level of the eusocial organisms (i.e., ants, honey bees) are those that are constantly present and individual organism and focus on physical but to include parental care and group-liv- therefore remain relatively static in the barriers (e.g., the honey bee cuticle) and ing species in general (Cotter & Kilner, background and do not change when individual physiological defenses that are 2010). Meunier (2015) further clarified individuals or colonies are exposed to largely induced in response to patho- this expansion to define social immu- pathogens. Inducible defenses are those gens that get past the initial defenses nity as any defense against parasites and that are activated upon the presence (e.g., antimicrobial peptides in the bee pathogens that evolved and is maintained of pathogens or parasites. All immune hemolymph). For honey bees (specifically due to the benefits derived by group defenses lie somewhere along this gradi- Apis mellifera in this discussion) and other members. In this way social immunity is ent, and each can play a crucial role in the social insects, however, the colony is often limited to traits that ultimately express at overall colony or social immune system. the unit of evolutionary selection (Seeley, least some level of benefit to the colony or 1997). Combined efforts of individual superorganism. This article aims to describe mechanisms honey bees promote colony productiv- of social immunity that honey bees use ity and survival; thus individuals in that Analogies can be made between mecha- to reduce the spread of pathogens and colony survive to successfully spread their nisms of individual and social immune parasites at the colony level. The initial genetics through subsequent generations defense, which also sheds light on the description and recent reviews of social via the production of drones, swarms, and superorganism concept (Cremer & Sixt, immunity tended to structure discussions queens. 2009). One clear example would be of the different defenses around parasite the analogy of cellular encapsulation, exposure (starting with limiting parasite In many ways, immunity in social which involves hemocytes in the bee’s uptake at the individual level and ending insects exemplifies the superorganism hemolymph surrounding a microbe that with reducing spread of pathogens within concept, whereby there is an immune has penetrated into a bee’s system. These and across colonies) (Cremer et al., 2007; system in individual bees, but there is cells surround the microbe and produce Meunier, 2015). In their foundational also a colony-level immune system. Both cytotoxic compounds to destroy it, thus work, Cremer and colleagues (2007) then function to promote survival not only of preventing it from further infecting the separated discussion within the defenses an individual bee but also of the colony. individual bee. This is analogous to what as “prophylactic measures and activated Given the reduction in immune genes happens in Apis ceranae japonica colonies responses;” here the term constitutive that has now been noted for honey bees that are attacked by the Japanese hornet replaces prophylactic and inducible and Hymenoptera in general (Barribeau (Vespula mandarinia japonica). These replaces activated to merge the terminol- et al., 2015; Evans et al., 2006; Gadau et hornets invade the honey bee colony ogies associated with physiological immu- al., 2012; Simola et al., 2013), it seems and individual bees (e.g., the cellular nity and better facilitate connections with as though the evolution of numerous colo- hemocytes of the superorganism) tightly descriptions of social immunity. Moving ny-level, largely behavioral mechanisms surround and “ball” the hornet, killing forward in the discussion of the evolution has occurred either to compensate for it by generating heat and carbon dioxide of social immune defenses, investigations DOI: 10.1080/0005772X.2017.1307800 This work was authored as part of the Contributor's official duties as an Employee Bee World • VOL 94 • March 2017 • Page 21 of the United States Government and is therefore a work of the United States Government. In accordance with 17 USC. 105, no copyright protection is available for such works under US Law. REVIEW ARTICLE Figure 1. Overview of social immunity in honey bees. Traits are depicted on the continuum from highly constitutive (prophylactic) to highly inducible (activated by pathogen exposure). All photos were taken by M. Simone-Finstrom. into how colonies invest in constitutive unless the colony replaces that queen. a large number of males (i.e., more than versus inducible defenses should be at the Given this, genetic diversity plays a back- 5–7) (Palmer & Oldroyd, 2000). Rearing forefront. As there are costs and benefits ground role in colony health and produc- queens from the youngest larvae available associated with reliance on different types tivity, albeit a significant one. Colonies results in larger queens that, on average, of defenses, this aspect needs to be more with increased levels of genetic diversity mate with more males (Tarpy, Hatch, fully considered with respect to social have been shown to have increased forag- & Fletcher, 2000; Tarpy, Keller, Caren, immunity as it has for individual, physi- ing efficiency (Eckholm, Anderson, Weiss, & Delaney, 2011) and thus have more ological immunity (Adamo, Davies, Easy, & DeGrandi-Hoffman, 2011), healthier productive colonies (Rangel, Keller, & Kovalko, & Turnbull, 2016; Hamilton, gut microbial communities (Mattila, Rios, Tarpy, 2013). This is one way to promote Siva-Jothy, & Boots, 2008; Westra et al., Walker-Sperling, Roeselers, & Newton, increased genetic diversity in managed 2015). With this in mind, the review pre- 2012), overall increased fitness and colonies. In addition, ensuring adequate sented here uses the gradient of constitu- productivity (Mattila & Seeley, 2007), and drone sources in mating yards is key for a tive effects to induced effects (Figure 1) as better survival in commercial beekeeping queen to have access to large numbers of the framework for discussion. operations (Tarpy et al., 2013). From a males during her mating flights. disease perspective, colonies with higher levels of genetic diversity are more resist- Polyandry and the Case ant to disease and have infections of less Task Allocation for Genetic Diversity intensity (Bailey, 1999; Tarpy, 2003; Tarpy In addition to promoting task efficiency, & Seeley, 2006). This at least in part could Honey bees colonies are headed by one the division of labor among workers has be due to larval immunity (Invernizzi, queen that mates early in her life with a constitutive effect against the spread of Penagaricano, & Tomasco, 2009; Palmer numerous different males (Ruttner, 1956), pathogens and parasites within colonies. & Oldroyd, 2003; Simone-Finstrom, Walz, and is responsible for producing all of Honey bee task is largely guided by bee & Tarpy, 2016) or even general immuno- the workers that comprise the colony. age, which is known as temporal polye- competence (López-Uribe, Appler, Dunn, Multiple mating of the queen is referred thism. Typically
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