Reproductive Potential Impacts Body Maintenance Parameters and Global DNA Methylation in Honeybee Workers (Apis mellifera L.)

SIMPLE SUMMARY: The queens and sterile workers arise from genetically identical eggs but as imagoes, they differ in their life span, DNA methylation, and their functions. In the absence of the queen, the larvae develop into rebels, i.e., workers with increased reproductive potential. We assumed that since rebels are similar to the queen in many anatomical and behavioral features, they live longer and have lower levels of global DNA methylation, even when infected, e.g., by Nosema spp. Rebels always lived longer in comparison in normal workers and unexpectedly extended longevity of normal workers when they were together, similarly as the presence of a queen did. Rebels became infected more easily but tolerated the infection better. They also had lower level of global DNA methylation than normal workers. These features expand possibilities of the use of honeybees as a model for studies on senescence, nosemosis, eusocial evolution, and epigenetics. ABSTRACT: The widely accepted hypothesis in life history evolution about the trade-off between fecundity and longevity is not confirmed by long-living and highly fecund queens in eusocial insects. The fact that the queens and facultatively sterile workers usually arise from genetically identical eggs but differ in DNA methylation makes them a good model for studies on senescence, eusocial evolution, and epigenetics. Therefore, honeybees seem to be especially useful here because of long living rebel-workers (RW) with high reproductive potential recently described. Longevity, ovariole number, nosema tolerance, and global DNA methylation have been assayed in normal workers (NW) versus RW in hives and cages. RW always lived longer than NW and unexpectedly extended longevity of NW when they were together, similarly as the presence of a queen did. RW lived longer despite the fact that they had higher Nosema spore load; surprisingly they became infected more easily but tolerated the infection better. Global DNA methylation increased with age, being lower in RW than in NW. Therefore, RW are queen-like considering global DNA methylation and the link between fecundity, longevity, and body maintenance. Presented features of RW expands possibilities of the use of honeybees as a model for studies on senescence, nosemosis, eusocial evolution, and epigenetics.