Social Evolution With Decoupling of Multiple Roles of Biogenic Amines Into Different Phenotypes in Hymenoptera

Abstract

Convergent evolution of eusociality with the division of reproduction and its plastic transition in Hymenoptera has long attracted the attention of researchers. To explain the evolutionary scenario of the reproductive division of labor, several hypotheses had been proposed. Among these, we focus on the most basic concepts, i.e., the ovarian ground plan hypothesis (OGPH) and the split-function hypothesis (SFH). The OGPH assumes the physiological decoupling of ovarian cycles and behavior into reproductive and non-reproductive individuals, whereas the SFH assumes that the ancestral reproductive function of juvenile hormone (JH) became split into a dual function. Here, we review recent progress in the understanding of the neurohormonal regulation of reproduction and social behavior in eusocial hymenopterans, with an emphasis on biogenic amines. Biogenic amines are key substances involved in the switching of reproductive physiology and modulation of social behaviors. Dopamine has a pivotal role in the formation of reproductive skew irrespective of the social system, whereas octopamine and serotonin contribute largely to non-reproductive social behaviors. These decoupling roles of biogenic amines are seen in the life cycle of a single female in a solitary species, supporting OGPH. JH promotes reproduction with dopamine function in primitively eusocial species, whereas it regulates non-reproductive social behaviors with octopamine function in advanced eusocial species. The signal transduction networks between JH and the biogenic amines have been rewired in advanced eusocial species, which could regulate reproduction in response to various social stimuli independently of JH action.

Octopamine receptor gene influences social grouping in the masked birch caterpillar

“…Our current study extends the evidence that octopamine signaling acts as a driver of social behavioral transitions to the Lepidoptera. It should be noted that other biogenic amines such as dopamine and serotonin are also involved in mediating various insect social behaviours (e.g., [ 26 – 28 ]) and the interactions among the different amines including octopamine could be involved in shaping larval grouping behavior; however, exploring these molecular mechanisms is beyond the scope of this study. Our results confirm that the feeding dsRNA to Lepidoptera can trigger RNAi.…”

Environmentally responsive reproduction: neuroendocrine signalling and the evolution of eusociality

“…In D. melanogaster , ecdysis-triggering hormone (ETH) is also a key component of the neuroendocrine system regulating oogenesis and female fecundity [8••] . These hormones, together with biogenic amines and insulin signalling 7 , 9 , 10 , act to regulate oogenesis [11] ( Figure 1 ). However, the exact roles of these components in oogenesis vary widely among insect orders and even between closely related species.…”

“…The mechanism of action of these pheromones and how they inhibit reproduction in workers is, as yet, largely unknown. However, neuroendocrine signalling may play a key role, for example, JH is associated with reproduction in the wasp Vespula vulgaris [74] and dopamine has been found to correlate positively with reproduction in queenless worker bumblebees, paper wasps and some ants (reviewed in [75] ). However, more studies are required to link pheromone exposure with the underlying molecular mechanisms that repress reproduction to determine how these pheromones function and how they might have evolved.…”

Behavioral roles of biogenic amines in bumble bee males

“…Biogenic amines are physiological agents that function as neurotransmitters, neuromodulators, and neurohormones in various insect species [13][14][15][16][17] . These substances are involved in the age-related division of labor in honey bee workers 18,19 and the reproductive behavior of virgin queens 20,21 .…”