Social immunity in honey bees (Apis mellifera): transcriptome analysis of varroa-hygienic behaviour

Authors: CONTE, YVES - Institut National De La Recherche Agronomique (INRA); ALAUX, CEDRIC - Institut National De La Recherche Agronomique (INRA); MARTIN, JEAN-FRANCOIS - Institut National De La Recherche Agronomique (INRA); HARBO, JOHN - Retired ARS Employee; Harris, Jeffrey; DANTEC, CHRISTELLE - Institut National De La Recherche Agronomique (INRA); SEVERAC, DANNY - Institut National De La Recherche Agronomique (INRA); CROS-ARTEIL, SANDRINE - Institut National De La Recherche Agronomique (INRA); NAVAJAS, MARIA - Institut National De La Recherche Agronomique (INRA)

Submitted to: Insect Molecular Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/10/2011
Publication Date: 3/24/2011
Citation: Conte, Y.L., Alaux, C., Martin, J., Harbo, J.R., Harris, J.W., Dantec, C., Severac, D., Cros-Arteil, S., Navajas, M. 2011. Social immunity in honey bees (Apis mellifera): transcriptome analysis of varroa-hygienic behaviour. Insect Molecular Biology. 20(3):399-408.

Interpretive Summary: In insects, defence against pathogens relies mainly on an efficient innate immunity that comprised both cellular and humoral reactions (e.g. phagocytosis, melanisation and secretion of antimicrobial peptides) (Hoffmann, 2003; Siva-Jothy et al., 2005). However, when living in groups, like social insects, the presence of stored resources and the close living quarters increase both the attractiveness for pathogens and disease transmission (Schmid-Hempel, 1998). Therefore, higher capacities to respond and defend against pathogens could be expected. A genome-wide analysis of immunity in the honey bee Apis mellifera, the only social insects with a fully sequenced-genome, actually showed that they possess only one-third the number of immune response genes known for solitary insects (i.e., fruit fly, mosquito and moth) (Evans et al., 2006). Since the reduction in genes involved the different steps of the immune response, honey bees appears to have a reduce capacity to respond and defend against pathogens. However, despite the wide-range of pathogens, social insects are still successful to resist disease, which suggests that others defence mechanisms might be involved. Indeed, in addition to the individual defences, social insects developed group-level strategies against parasites and pathogens. Such social immunity includes grooming, the use of antimicrobial materials for nest construction (e.g. resin) (Christe et al., 2003; Simone et al., 2009), social fever (Starks et al., 2000) or nest hygiene (see (Cremer et al., 2007) for a review). Since their description, many studies explored the behavioural mechanisms of those collective immune defence against pathogens (see the following reviews (Wilson-Rich et al., 2009; Cremer et al., 2007; Cremer & Sixt, 2009)), but the molecular basis and pathways remain largely unknown. The identification of genes that influence social immunity would not only improve our understanding of its mechanisms but also provide new insights into the evolution of collective defence in insect societies. Indeed, genes involved in social immunity might have replaced genes from individual immunity that have been loss during evolution of sociality in social insects and might be key factors for the defence against diseases. In honey bees (Apis mellifera), a well-known behavioural trait to fight against pathogens is the hygienic behaviour, which consists in the identification and removal of dead or infected larvae. Using the honey bee genome, we attempted to identify genes involved in this well-characterized behaviour, a main component of social immunity. Hygienic behaviour is directed toward dead brood, but also brood infected with bacteria or fungi (Boecking & Spivak, 1999), the greater wax moth, Galleria mellonella (Villegas & Villa, 2006; Corrêa-Marques & De Jong, 1998), the small hive beetle, Aethina tumida (Ellis et al., 2003; Neumann & Härtels, 2004) or the mite Varroa destructor, the parasite with the most pronounced effect on honey bee colonies. Indeed, development of the varroa population, reproducing in brood cells, often lead to the death of the colony (Le Conte et al., 2010). Since hygienic behaviour is genetically-controlled (Rothenbuhler, 1964b; Rothenbuhler, 1964a), selective breeding for varroa resistance through increased varroa-hygienic behaviour offers a sustainable means for controlling mite parasitism. Different varroa-hygienic lines have been thus successfully bred (Harbo & Harris, 1999; Büchler et al., 2010; Harbo & Harris, 2005a; Boecking & Spivak, 1999; Spivak & Reuter, 2001a) and one of those is characterized by a low percentage of reproducing varroa mites. Bees from those colonies display an effective removal of mites with offspring from capped brood cells, which limits varroa infestation rate and reproduction (Harbo & Harris, 2005b; Harbo & Harris, 2009). This genetic line called varroa-

Technical Abstract: Honey bees tend to have a reduced number of immune genes compared to solitary insects. They actually developed an alternative collective defence consisting in the cooperation of individuals to decrease disease development. We identified a set of genes involved in this social immunity by comparing brain transcriptome of highly varroa-hygienic bees to normal bees. The function of those candidate genes doesn’t seem to support a higher olfactory sensitivity in hygienic bees, as previously hypothesized. However, comparing their gene expression profile with genomic profiles from others behaviours suggest a link with brood care and Africanized honey bees, who are also highly varroa-hygienic. These results represent a first step toward the identification of genes involved in social immunity that might have replaced genes involved in individual immunity and thus provide first insights into the evolution of social immunity.