Evolution of the Yellow/Major Royal Jelly Protein family and the emergence of social behavior in honey bees

Abstract

The genomic architecture underlying the evolution of insect social behavior is largely a mystery. Eusociality, defined by overlapping generations, parental brood care, and reproductive division of labor, has most commonly evolved in the Hymenopteran insects, including the honey bee Apis mellifera. In this species, the Major Royal Jelly Protein (MRJP) family is required for all major aspects of eusocial behavior. Here, using data obtained from the A. mellifera genome sequencing project, we demonstrate that the MRJP family is encoded by nine genes arranged in an ∼60-kb tandem array. Furthermore, the MRJP protein family appears to have evolved from a single progenitor gene that encodes a member of the ancient Yellow protein family. Five genes encoding Yellow-family proteins flank the genomic region containing the genes encoding MRJPs. We describe the molecular evolution of these protein families. We then characterize developmental-stage-specific, sex-specific, and caste-specific expression patterns of the mrjp and yellow genes in the honey bee. We review empirical evidence concerning the functions of Yellow proteins in fruit flies and social ants, in order to shed light on the roles of both Yellow and MRJP proteins in A. mellifera. In total, the available evidence suggests that Yellows and MRJPs are multifunctional proteins with diverse, context-dependent physiological and developmental roles. However, many members of the Yellow/MRJP family act as facilitators of reproductive maturation. Finally, it appears that MRJP protein subfamily evolution from the Yellow protein family may have coincided with the evolution of honey bee eusociality.

DNA methylation is widespread and associated with differential gene expression in castes of the honeybee, Apis mellifera

“…We further expanded our analyses to genes implicated in A. mellifera caste differentiation identified by previous studies of gene expression (33)(34)(35)(36)(37)(38). Again we found that caste-specific genes overwhelmingly belong to the high-CpG class ( Table 3).…”

The effect of different dietary sugars and honey on longevity and fecundity in two hyperparasitoid wasps

“…The most dominant protein found in honey produced by two honeybees within the genus Apis is rayalactin or Major Royal Jelly Protein 1 (MRJP1) (Won et al, 2008). One of the many functions of this protein involves the stimulation of reproductive maturation in honeybees (Drapeau et al, 2006). However, the sole action of MRJP1 in honeybees was found to be responsible for queen differentiation in which juvenile hormone titers increased and vitellogenin genes (precursors of yolk protein) were expressed at a higher rate.…”

Honey and royal jelly, like human milk, abrogate lectin-dependent infection-preceding Pseudomonas aeruginosa adhesion

“…Apalbumin 1 was reported to constitute 48% of the RJ proteins and also to be present in honey (Scarselli et al, 2005). The genes of those proteins were recently identified (Schmitzova et al, 1998;Drapeau et al, 2006) with the unveiling of the honeybee complete genome, and they are suggested to be multifunctional, performing diverse nutritional, physiological and developmental roles and affecting various tissues, including the brain (Drapeau et al, 2006).…”

“…For up to 3 days, the larvae are supplied with royal jelly (RJ) that is secreted by young worker bees (nurse bees) in the hive. Thereafter, only larvae designated to become queens receive RJ, while a mixture of honey, pollen and water is fed to larvae selected to become workers (Drapeau et al, 2006).…”