Abstract
Honeybees, Apis mellifera, show age-related division of labor in which young adults perform maintenance (“housekeeping”) tasks inside the colony before switching to outside foraging at approximately 23 days old. Disease resistance is an important feature of honeybee biology, but little is known about the interaction of pathogens and age-related division of labor. We tested a hypothesis that older forager bees and younger “house” bees differ in susceptibility to infection. We coupled an infection bioassay with a functional analysis of gene expression in individual bees using a whole genome microarray. Forager bees treated with the entomopathogenic fungus Metarhizium anisopliae s.l. survived for significantly longer than house bees. This was concomitant with substantial differences in gene expression including genes associated with immune function. In house bees, infection was associated with differential expression of 35 candidate immune genes contrasted with differential expression of only two candidate immune genes in forager bees. For control bees (i.e. not treated with M. anisopliae) the development from the house to the forager stage was associated with differential expression of 49 candidate immune genes, including up-regulation of the antimicrobial peptide gene abaecin, plus major components of the Toll pathway, serine proteases, and serpins. We infer that reduced pathogen susceptibility in forager bees was associated with age-related activation of specific immune system pathways. Our findings contrast with the view that the immunocompetence in social insects declines with the onset of foraging as a result of a trade-off in the allocation of resources for foraging. The up-regulation of immune-related genes in young adult bees in response to M. anisopliae infection was an indicator of disease susceptibility; this also challenges previous research in social insects, in which an elevated immune status has been used as a marker of increased disease resistance and fitness without considering the effects of age-related development.
Highlights
Declining populations of honeybees, Apis mellifera, have been recorded in many countries, causing widespread concern [1,2]
House bees and forager bees (26 days old) showed differences in the rate at which they succumbed to lethal infections of the entomopathogenic fungus M. anisopliae s.l. in a laboratory bioassay
Quantification of M. anisopliae 18S rRNA by RTPCR indicated that the fungus was present at significantly higher levels in M. anisopliaetreated house bees at 48 hrs post inoculation compared to M. anisopliae-treated forager bees (DCt = 2.65, t22 = 14.5, p,0.001)
Summary
Apis mellifera, have been recorded in many countries, causing widespread concern [1,2]. Honeybees have a highly developed form of social organization, characterized by the presence of overlapping generations within the colony, cooperative care of offspring, and reproductive division of labor [5,6]. Their success can be attributed to living in large, organized colonies which improves their ability to compete for resources against small groups or solitary species [7]. Honeybees – like other eusocial insects – invest heavily in pathogen defense [9].
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