Rapid juvenile hormone downregulation in subordinate wasp queens facilitates stable cooperation

Abstract

In many cooperatively breeding animals, subordinate group members have lower reproductive capacity than dominant group members. Theory suggests subordinates may downregulate their reproductive capacity because dominants punish subordinates who maintain high fertility. However, there is little direct experimental evidence that dominants cause physiological suppression in subordinates. Here, we experimentally test how social interactions influence subordinate reproductive hormones in paper wasps. queens commonly found nests in cooperative groups where the dominant queen is more fertile than the subordinate queen. In this study, we randomly assigned wasps to cooperative groups, assessed dominance behaviour during group formation, then measured levels of juvenile hormone (JH), a hormone that mediates fertility. Within three hours, lowest ranking subordinates had less JH than dominants or solitary controls, indicating that group formation caused rapid JH reduction in low-ranking subordinates. In a second experiment, we measured the behavioural consequences of experimentally increasing subordinate JH. Subordinates with high JH-titres received significantly more aggression than control subordinates or subordinates from groups where the dominant's JH was increased. These results suggest that dominants aggressively punished subordinates who attempted to maintain high fertility. Low-ranked subordinates may rapidly downregulate reproductive capacity to reduce costly social interactions with dominants. Rapid modulation of subordinate reproductive physiology may be an important adaptation to facilitate the formation of stable, cooperative groups.

Diversity of Insect Sesquiterpenoid Regulation

“…It is worth also noting that the response to JH could be different among members of the same colony. In Polistes canadensis , the effect of JH on ovaries are different between queens and workers as a potential trophic advantage of the queens over the workers ( Giray et al, 2005 ), while in Polistes dominulus where queens nest cooperatively with other queens, JH has a stronger effect on the dominance, fertility, and aggressiveness of large queens ( Tibbetts and Izzo, 2009 ; Tibbetts et al, 2011 , 2018 ). In species Polistes metricus with non-cooperative nest-founding queen pattern, JH leads to an increase of fertility for all individuals, but among the cooperative workers, large workers increase their fertility in response to JH more while small workers do not ( Tibbetts and Sheehan, 2012 ).…”

Distributed physiology and the molecular basis of social life in eusocial insects

“…This evolutionary history is reflected today by the partitioned expression of the same genome between workers and queens 29,119,120 . This plastic state is still observed in species considered to be "facultatively social" (note that this label does not imply that all social species progress along similar or predictable evolutionary paths 18 122 , control of nutritional intake 123 , and multiple modes of physical interaction such as piping and drumming 124 . In various ant and bee species, secretions passed among workers and queens can influence the fertility of all engaged actors, and thus influence colony productivity overall.…”

Pre-existing differences in putative fertility signals give workers the upper hand in ant reproductive hierarchies

“…Lamba et al (2007) hypothesized that in other eusocial insects (wasps) fighting could be used not to exclude the other females from dominance, but rather to speed up the development of the ovarian system of the future reproductive (via an action on biogenic amines) and so facilitate the monopolization of colony reproduction. Aggressive behaviours also lead to a decrease in juvenile hormone titre (usually positively correlated with fertility) in subordinate individuals (Tibbetts et al, 2018). Physical contact between workers in the ant Diacamma has also been shown to affect dopamine secretion in the worker's brain and to regulate reproduction inside the nest (Shimoji et al, 2017).…”

“…Agonistic interactions acting on the physiological and hormonal secretions would reinforce the preexisting differences in fertility between individuals, and this would accelerate cooperation within the nest. Subordinates would maximize their fitness by quickly resolving conflicts by reducing their ability to reproduce (Tibbetts et al, 2018).…”