Immunosenescence in honey bees (Apis mellifera L.) is caused by intrinsic senescence and behavioral physiology

Author(s)

Lourenco, Anete Pedro ^{[1, 2]} ; Martins, Juliana Ramos ^[1] ; Silva Torres, Fernanda Andrade ^{[3, 1]} ; Mackert, Aline ^{[3, 4]} ; Aguiar, Luiz Roberto ^[1] ; Hartfelder, Klaus ^[5] ; Gentile Bitondi, Marcia Maria ^[3] ; Paulino Simoes, Zila Luz ^[3]

Affiliation

^[1] Univ Sao Paulo, Fac Med Ribeirao Preto, Dept Genet, Ribeirao Preto, SP - Brazil

^[2] Univ Fed Vales Jequitinhonha & Mucuri, Dept Ciencias Biol, Fac Ciencias Biol & Saude, Campus JK, Rodovia MGT 367, Km 583, BR-39100000 Diamantina, MG - Brazil

^[3] Univ Sao Paulo, Fac Filosofia Ciencias & Letras Ribeirao Preto, Dept Biol, Ribeirao Preto, SP - Brazil

^[4] Univ Fed Mato Grosso do Sul, Dept Ciencias Ambiente, Campus Pantanal, Corumba, MS - Brazil

^[5] Univ Sao Paulo, Fac Med Ribeirao Preto, Dept Biol Celular & Mol & Bioagentes Patogen, Ribeirao Preto, SP - Brazil

• Document type: Journal article
• Source: Experimental Gerontology; v. 119, p. 174-183, MAY 2019.
• Web of Science Citations: 1

Abstract

Young honey bee workers (0 to 2-3 weeks old) perform tasks inside the colony, including brood care (nursing), whereas older workers undergo foraging tasks during the next 3-4 weeks, when an intrinsic senescence program culminates in worker death. We hypothesized that foragers are less able to react to immune system stimulation than nurse bees and that this difference is due to an inefficient immune response in foragers. To test this hypothesis, we used an experimental design that allowed us to uncouple chronological age and behavior status (nursing/foraging). Worker bees from a normal age demography colony (where workers naturally transit from nursing to foraging tasks as they age) and of a single-cohort colony setup (composed of same-aged workers performing nursing or foraging tasks) were tested for survival and capability of activation of the immune system after bacterial injection. Expression of an antimicrobial peptide gene, defensin-1 (def-1), was used to assess immune system activation. We then checked whether the immune response includes changes in the expression of aging- and behavior-related genes, specifically vitellogenin (vg), juvenile hormone esterase (jhe), and insulin-like peptide-1 (ilp-1). We found a significant difference in survival rate between bees of different ages but carrying out the same tasks. Our results thus indicate that the bees' immune response is negatively affected by intrinsic senescence. Additionally, independent of age, foragers had a shorter lifespan than nurses after bacterial infection, although both were able to induce def-1 transcription. In the normal age demography colony, the immune system activation resulted in a reduction in the expression of vg, jhe and ilp-1 genes in foragers, but not in the nurse bees, demonstrating that age and behavior are both important influences on the bees' immune response. By disentangling the effects of age and behavior in the single-cohort colony, we found that vg, jhe and ilp-1 response to immune system stimulation was independent of behavior. Younger bees were able to mount a stronger immune response than older bees, thus highlighting age as an important factor for immunity. Taken together, our results provide new insights into how age and behavior affect the honey bee's immune response. (AU)

• FAPESP's process: 05/03302-1 - Apis mellifera hexamerin HEX 70c: cDNA characterization and expression during metamorphosis and reproduction
• Grantee: Juliana Ramos Martins
• Support Opportunities: Scholarships in Brazil - Master
• FAPESP's process: 05/03926-5 - Functional genomics of Apis mellifera: search for new genes and functional networks in the context of development, different castes and reproduction
• Grantee: Zilá Luz Paulino Simões
• Support Opportunities: Research Projects - Thematic Grants
• FAPESP's process: 11/03171-5 - Causal analysis of Apis mellifera development: regulatory genes and hierachical networks of gene expression in the specification of tissue and organs
• Grantee: Zilá Luz Paulino Simões
• Support Opportunities: Research Projects - Thematic Grants