Royal decree: gene expression in transgenerationally immune primed bumblebee workers mimics a primary immune response

Invertebrates lack the cellular and physiological machinery of the adaptive immune system, but show specificity in their immune response [1, 2] and immune priming [3-11]. Functionally, immune priming is comparable to immune memory in vertebrates. Individuals that have survived exposure to a given parasite are better protected against subsequent exposures. Protection may be cross-reactive (e.g. [12]), but demonstrations of persistent and specific protection in invertebrates are increasing [3, 5]. This immune priming can cross generations ("trans-generational" immune priming) [4, 8], preparing offspring for the prevailing parasite environment. While these phenomena gain increasing support, the mechanistic foundations underlying such immune priming, both within and across generations, remain largely unknown. Using a transcriptomic approach, we show a bacterial challenge to bumblebee queens, known to induce trans-generational immune priming, alters daughter (worker) gene expression. Daughters, even when unchallenged themselves, constitutively express a core set of the genes induced upon direct bacterial exposure, including high expression of antimicrobial peptides, a beta-glucan receptor protein implicated in bacterial recognition and the induction of the toll signaling pathway[13], and slit-3 which is important in honeybee immunity[14]. Maternal challenge results in a distinct upregulation of their daughters' immune system, with a signature overlapping with the induced individual response to a direct immune challenge. This will mediate mother-offspring protection, but also associated costs related to reconfiguration of constitutive immune expression. Identification of conserved immune pathways in memory-like responses has important implications for our understanding of the innate immune system, including the innate components in vertebrates, which share many of these pathways[15].