Maternal Effect on Female Caste Determination in a Social Insect

Abstract

Caste differentiation and division of labor are the hallmarks of social insect colonies [1, 2]. The current dogma for female caste differentiation is that female eggs are totipotent, with morphological and physiological differences between queens and workers stemming from a developmental switch during the larval stage controlled by nutritional and other environmental factors (e.g., [3-8]). In this study, we tested whether maternal effects influence caste differentiation in Pogonomyrmex harvester ants. By conducting crossfostering experiments we identified two key factors in the process of caste determination. New queens were produced only from eggs laid by queens exposed to cold. Moreover, there was a strong age effect, with development into queens occurring only in eggs laid by queens that were at least two years old. Biochemical analyses further revealed that the level of ecdysteroids was significantly lower in eggs developing into queens than workers. By contrast, we found no significant effect of colony size or worker exposure to cold, suggesting that the trigger for caste differentiation may be independent of the quantity and quality of resources provided to larvae. Altogether these data demonstrate that the developmental fate of female brood is strongly influenced by maternal effects in ants of the genus Pogonomyrmex.

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

“…These results reveal a role of JH in the regulation of caste polyphenism in P. rugosus. In this species, maternal effects were previously found to stimulate the production of queens in response to hibernation, as only colonies headed by a hibernated queen produced queens, whether or not the workers had been exposed to cold (45). The exposure to cold therefore triggers changes in queens that make them more likely to lay queen-destined eggs.…”

“…Interestingly, the results revealed a trend toward a reduction of 20E titer in methoprene-treated queens and a significant negative relationship between the 20E titer in queens and the proportion of queens in their offspring. This suggests that ecdysteroids may be involved in the process of caste determination (45,93).…”

“…In ants, several studies suggested that maternal factors such as temperature or queen age may affect caste determination (40)(41)(42)(43)(44). However, it is only recently that the first example of maternal effects on female caste polyphenism was documented experimentally (45). Cross-fostering of eggs between hibernated and nonhibernated Pogonomyrmex colonies revealed strong maternal effects on caste production, as only eggs produced by a hibernated queen were able to develop into queens, irrespective of the hibernation status of the rest of the colony (45).…”

“…However, it is only recently that the first example of maternal effects on female caste polyphenism was documented experimentally (45). Cross-fostering of eggs between hibernated and nonhibernated Pogonomyrmex colonies revealed strong maternal effects on caste production, as only eggs produced by a hibernated queen were able to develop into queens, irrespective of the hibernation status of the rest of the colony (45). Such maternal effects on the caste fate of the female offspring require that the hibernation triggers changes in the queen that affect polyphenism in the offspring.…”

“…Such maternal effects on the caste fate of the female offspring require that the hibernation triggers changes in the queen that affect polyphenism in the offspring. Hormones may be involved in this process in Pogonomyrmex ants, as Pogonomyrmex rugosus queen-and worker-destined eggs differed in their ecdysteroid content (45) and Pogonomyrmex barbatus mature queens treated with juvenile hormone (JH) were recently found to produce larger workers (46).…”