She's got nerve: roles of octopamine in insect female reproduction

Abstract

The biogenic monoamine octopamine (OA) is a crucial regulator of invertebrate physiology and behavior. Since its discovery in the 1950s in octopus salivary glands, OA has been implicated in many biological processes among diverse invertebrate lineages. It can act as a neurotransmitter, neuromodulator and neurohormone in a variety of biological contexts, and can mediate processes including feeding, sleep, locomotion, flight, learning, memory, and aggression. Here, we focus on the roles of OA in female reproduction in insects. OA is produced in the octopaminergic neurons that innervate the female reproductive tract (RT). It exerts its effects by binding to receptors throughout the RT to generate tissue- and region-specific outcomes. OA signaling regulates oogenesis, ovulation, sperm storage, and reproductive behaviors in response to the female's internal state and external conditions. Mating profoundly changes a female's physiology and behavior. The female's OA signaling system interacts with, and is modified by, male molecules transferred during mating to elicit a subset of the post-mating changes. Since the role of OA in female reproduction is best characterized in the fruit fly Drosophila melanogaster, we focus our discussion on this species but include discussion of OA in other insect species whenever relevant. We conclude by proposing areas for future research to further the understanding of OA's involvement in female reproduction in insects.

Keywords: Octopamine; fertility; insect; reproduction.

Figure 1

Octopamine biosynthetic pathway and classification of octopamine receptors. A Tyrosine decarboxylase (TDC) converts tyrosine to tyramine by decarboxylation. Tyramine is hydroxylated by tyramine β-hydroxylase (TBH) to produce octopamine. B Classification of octopamine receptors based on schemes from Evans and Maqueira (2005), Farooqui (2012), Wu (2014), and Hana and Lange (2017). OA=octopamine, TA=Tyramine, cAMP=cyclic adenosine monophosphate, Ca²⁺=Calcium.

Figure 2

Features of the insect female reproductive tract. A Diagram of the Drosophila melanogaster female reproductive tract (top) and the Locusta migratoria female reproductive tract (bottom). L. migratoria diagram based on (Lange 2009b). D. melanogaster diagram based on (Miller 1950). B Locations of Tdc2⁺ dsx⁺ neurons and SPSNs in the D. melanogaster female reproductive tract and VNC. Circle depicts cell bodies and ‘v’ shapes depict innervations.

Figure 3

Summary of octopamine functions within the Drosophila melanogaster female reproductive tract. Red lines on the ovary represent the peritoneal sheath musculature. Colored boxes on the sides illustrate signaling pathways in specific regions of the reproductive tract.