Interplay between Insulin Signaling, Juvenile Hormone and Vitellogenin Regulates Maternal Effects on Polyphenism in Ants

Authors: LIBBRECHT, ROMAIN - University Of Lausanne; Corona, Miguel; AZEVEDO, DIHEGO - Universidade Federal De Vicosa; SERRAO, JOSE - Universidade Federal De Vicosa; KELLER, LAURENT - University Of Lausanne

Submitted to: PLoS Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/22/2013
Publication Date: 3/28/2013
Citation: Libbrecht, R., Corona, M.V., Azevedo, D., Serrao, J.E., Keller, L. 2013. Interplay between Insulin Signaling, Juvenile Hormone and Vitellogenin Regulates Maternal Effects on Polyphenism in Ants. PLoS Biology. 110(27):11050-11055.

Interpretive Summary: In honey bees, it has been well-established that the development of honeybee female larvae to queen or worker is not genetically determined, but regulated by the differential nutrition that the developing larvae receive from the nurse bees. In ants, the genetic and nutritional influences on the caste determination process are less clear. Whereas there is positive evidence that in some species caste determination is regulated by nutrition, in other ants, such as the harvester ant Pogonomyrmex barbatus, it has been reported that caste determination is genetically determined. In this study we show that in P. barbatus hibernation determines the amount of vitellogenin (Vg) in the eggs that the queens produce, which in turn determines the fate of an egg into queen or worker. Vg is a yolk protein that is used as a source of amino acids for the developing embryo. We propose that the amount of Vg in the eggs, replaces the function of nourishment provided by the nurses in other ants and honey bees. This report reveals a novel mechanism of caste determination in ants and suggests the possibility that similar maternal effects could take place in other social insects, including honey bees. This research supports the hypothesis that the size of the egg (and its vitellogenin content) has a potential effect on the size and productivity of adult queen bees.

Technical Abstract: Polyphenism is the phenomenon where alternative phenotypes are produced by a single genotype in response to environmental cues. An extreme case is found in social insects, where reproductive queens and sterile workers that greatly differ in morphology and behavior can arise from a single genotype. The first experimental evidence for maternal effects on caste determination, the differential larval development toward the queen or worker caste, was recently documented in Pogonomyrmex seed-harvester ants, in which only colonies with a hibernated queen produce new queens. However, the proximate mechanisms behind these intergenerational effects have remained elusive. We used a combination of artificial hibernation, hormonal treatments, gene expression analyses and vitellogenin quantification to investigate how the combined effect of environmental cues and hormonal signaling affects the process of caste determination in Pogonomyrmex ants. The results show that the interplay between insulin signaling, juvenile hormone and vitellogenin regulates maternal effects on the production of alternative phenotypes and set vitellogenin as a likely key player in the intergenerational transmission of information. This study reveals how hibernation triggers the production of new queens in Pogonomyrmex ant colonies. More generally, it shows how environmental cues experienced by one generation can translate into phenotypic variation in the next generation.