Social dominance and reproductive differentiation mediated by dopaminergic signaling in a queenless ant

Abstract

In social Hymenoptera with no morphological caste, a dominant female becomes an egg layer, whereas subordinates become sterile helpers. The physiological mechanism that links dominance rank and fecundity is an essential part of the emergence of sterile females, which reflects the primitive phase of eusociality. Recent studies suggest that brain biogenic amines are correlated with the ranks in dominance hierarchy. However, the actual causality between aminergic systems and phenotype (i.e. fecundity and aggressiveness) is largely unknown due to the pleiotropic functions of amines (e.g. age-dependent polyethism) and the scarcity of manipulation experiments. To clarify the causality among dominance ranks, amine levels and phenotypes, we examined the dynamics of the aminergic system during the ontogeny of dominance hierarchy in the queenless ant Diacamma sp., which undergoes rapid physiological differentiation based on dominance interactions. Brain dopamine levels differed between dominants and subordinates at day 7 after eclosion, although they did not differ at day 1, reflecting fecundity but not aggressiveness. Topical applications of dopamine to the subordinate workers induced oocyte growth but did not induce aggressiveness, suggesting the gonadotropic effect of dopamine. Additionally, dopamine receptor transcripts (dopr1 and dopr2) were elevated in the gaster fat body of dominant females, suggesting that the fat body is a potential target of neurohormonal dopamine. Based on this evidence, we suggest that brain dopamine levels are elevated in dominants as a result of hierarchy formation, and differences in dopamine levels cause the reproductive differentiation, probably via stimulation of the fat body.

Ant circadian activity associated with brood care type

“…Each colony was reared in plastic artificial nests filled with moistened plaster. This rearing method and the general biology of this species are available in [20,22]. The nests were maintained at 258C under 16 L : 8 D (light phase, 0700 -2300).…”

“…Diacamma colonies consist of one mated egg-layer (i.e. gamergate) and 30 -200 workers which perform agedependent division of labour [19,20]. Their nurses exhibit clear circadian activity rhythms when individually isolated from a colony (active in daytime) [19].…”

Social dominance alters nutrition‐related gene expression immediately: transcriptomic evidence from a monomorphic queenless ant

“…Five orphan colonies (lacking gamergates), each containing 15 workers, were made from three original colonies, as described previously (Okada et al . , ). Under natural conditions, such small colonies are often observed, and they are probably excavated soon after fission (Y. Okada, personal observation).…”

“…(a) If a callow female retains the wing‐like appendages called ‘gemmae’, she becomes a future reproductive so that her aggressive dominance behaviour remains at a high level [red dashed line (Okada et al . ), and her ovaries rapidly develop (red solid line and illustration (Okada et al . )].…”

Dopamine in socioecological and evolutionary perspectives: implications for psychiatric disorders

“…Recent studies have shown that DA plays an important role in social hierarchy of ants, with DA concentration significantly higher in socially dominants than subordinates (Penick et al, 2014; Okada et al, 2015). A similar observation has also been reported in a bird such as ring-necked phesants, with higher social rank males exhibiting higher striatal DA concentration (Mcintyre and Chew, 1983).…”