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

Ken Sasaki,Kazuki Tsuji,Hiroyuki Shimoji,Toru Miura,Yasukazu Okada,Hitoshi Aonuma

doi:10.3389/fevo.2021.659160

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.

Highlights

Eusociality in insects, characterized by sophisticated division of labor among group members, is assumed to have evolved convergently from non-eusocial ancestors in an individual taxon such as Hymenoptera, Blattodea, Hemiptera, Thysanoptera, and Coleoptera
The present paper discusses the evolutionary process of the reproductive division of labor from solitary to advanced eusociality, which is more related to ovarian ground plan hypothesis (OGPH) than reproductive ground plan hypothesis (RGPH)
The OGPH assumes the physiological decoupling of ovarian cycles and behavior into reproductive and non-reproductive states

Summary

INTRODUCTION

Eusociality in insects, characterized by sophisticated division of labor among group members, is assumed to have evolved convergently from non-eusocial ancestors in an individual taxon such as Hymenoptera (bees, wasps, and ants), Blattodea (termites), Hemiptera (aphids), Thysanoptera (thrips), and Coleoptera (beetles) (reviewed by Berens et al, 2015; Toth and Rehan, 2017; Costa, 2018). In advanced eusocial species, JH inhibits the synthesis of a precursor of egg yolk vitellogenin or does not affect ovarian development (Robinson and Vargo, 1997; Pinto et al, 2000; Bloch et al, 2009; Figure 1) These findings well fit the SFH that the ancestral reproductive function of JH became split into a dual function, regulating reproduction in queens and behavioral division of labor among workers. It is likely that foraging onset in worker bees is governed by redundant control mechanisms Such a JH function regulating the age-related division of labor has been reported in other advanced eusocial species such as the paper wasp Polybia occidentalis (O’Donnell and Jeanne, 1993) and some ants (Diacamma: Sommer et al, 1993; Harpegnathos saltator, Penick et al, 2011; Figure 1). In the ant Pristomyrmex punctatus, the intake of secretion of the myrmecophile butterfly Narathura japonica larvae causes a low level of brain dopamine that enhances the intensity of guarding behavior of workers to the latter (Hojo et al, 2015)

DISCUSSION

CONCLUSION