Interplay between insulin signaling, juvenile hormone, and vitellogenin regulates maternal effects on polyphenism in ants

Abstract

Polyphenism is the phenomenon in which alternative phenotypes are produced by a single genotype in response to environmental cues. An extreme case is found in social insects, in which reproductive queens and sterile workers that greatly differ in morphology and behavior can arise from a single genotype. 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, hormone measurements, and vitellogenin quantification to investigate how the combined effect of environmental cues and hormonal signaling affects the process of caste determination in Pogonomyrmex rugosus. 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 provides important information on maternal effects by showing how environmental cues experienced by one generation can translate into phenotypic variation in the next generation.

Pleiotropic effects of juvenile hormone in ant queens and the escape from the reproduction–immunocompetence trade-off

“…S. invicta might have escaped the RS trade-off using the alternative pathway by decoupling the regulatory effects of JH on the innate immune system instead of changing its regulatory role in reproduction. In a recent study, Libbrecht et al [46] document a similar function of JH of in queens of Pogonomyrmex rugosus. These results suggest that JH's function is not conserved in ants and can act as a flexible tool in regulating key systemic processes in different genera.…”

“…This effect would likely result in severe fitness costs to young queens during the critical founding stage. An alternative explanation for our findings might be related to the well-documented role of JH in regulating moulting and caste determination in insects [45,46]. As JHa is likely transferred to the larvae, it might have inhibited the moulting process of late larvae and consequently prevented pupation.…”

Modification of feeding circuits in the evolution of social behavior

“…Within colonies, nurses have higher Vg expression and more ovarioles than foragers, indicating that nurse bees performing brood care exhibit a reproductive physiology more similar to that of mothers despite being nonreproductive themselves . In addition, Vg and its interaction with juvenile hormone and insulin signaling regulate maternal effects on caste determination in ants (Libbrecht et al, 2013), and changes in Vg are associated with behavioral transitions to parental care in both male and female burying beetles (Parker et al, 2015;Roy-Zokan et al, 2015). In concert, these studies present evidence that mechanisms mediating maternal care have been selected upon during the evolution of sociality.…”

Caste development and evolution in ants: it's all about size

“…In P. pallidula, overwintered queens produce eggs with a potential for queen development, possibly due to increased JH in the eggs (Passera and Suzzoni, 1979). In Pogonomyrmex rugosus, queens must be both mature and overwintered to lay eggs with a potential for queen development, possibly due to differences in ecdysone or vitellogenin levels in the eggs (Schwander et al, 2008;Libbrecht et al, 2013).…”

“…In M. rubra, overwintered larvae have prolonged development, allowing them to attain larger size (Brian, 1956). In P. rugosus, only the first eggs laid by overwintered queens have the potential for queen development (Libbrecht et al, 2013). Overwintering is a discrete event, ubiquitous in temperate regions, so it may have been co-opted multiple times by natural selection to produce non-normal size−frequency distributions in ants.…”