Regulation of Mating-Induced Increase in Female Germline Stem Cells in the Fruit Fly Drosophila melanogaster

Abstract

In many insect species, mating stimuli can lead to changes in various behavioral and physiological responses, including feeding, mating refusal, egg-laying behavior, energy demand, and organ remodeling, which are collectively known as the post-mating response. Recently, an increase in germline stem cells (GSCs) has been identified as a new post-mating response in both males and females of the fruit fly, Drosophila melanogaster. We have extensively studied mating-induced increase in female GSCs of D. melanogaster at the molecular, cellular, and systemic levels. After mating, the male seminal fluid peptide [e.g. sex peptide (SP)] is transferred to the female uterus. This is followed by binding to the sex peptide receptor (SPR), which evokes post-mating responses, including increase in number of female GSCs. Downstream of SP-SPR signaling, the following three hormones and neurotransmitters have been found to act on female GSC niche cells to regulate mating-induced increase in female GSCs: (1) neuropeptide F, a peptide hormone produced in enteroendocrine cells; (2) octopamine, a monoaminergic neurotransmitter synthesized in ovary-projecting neurons; and (3) ecdysone, a steroid hormone produced in ovarian follicular cells. These humoral factors are secreted from each organ and are received by ovarian somatic cells and regulate the strength of niche signaling in female GSCs. This review provides an overview of the latest findings on the inter-organ relationship to regulate mating-induced female GSC increase in D. melanogaster as a model. We also discuss the remaining issues that should be addressed in the future.

Transcriptional Regulators of Ecdysteroid Biosynthetic Enzymes and Their Roles in Insect Development

“…In addition to PG, ovaries are known sites of ecdysteroid biosynthesis. Ovarian ecdysteroids are required for many aspects of oogenesis, such as the regulation of germline stem cell numbers, oocyte maturation, and follicle rupture ( Sieber and Spradling, 2015 ; Uryu et al, 2015 ; Ables and Drummond-Barbosa, 2017 ; Knapp and Sun, 2017 ; Yoshinari et al, 2019 ; Hoshino and Niwa, 2021 ) as well as for ovary-gut, and ovary-to-neuron communication ( Ahmed et al, 2020 ; Hadjieconomou et al, 2020 ; Zipper et al, 2020 ). Indeed, Halloween genes are expressed in ovarian follicle or nurse cells ( Chávez et al, 2000 ; Petryk et al, 2003 ; Niwa et al, 2004 , 2010 ; Warren et al, 2004 ; Namiki et al, 2005 ; Ono et al, 2006 ; Domanitskaya et al, 2014 ; Enya et al, 2014 ; Ameku and Niwa, 2016 ; Ameku et al, 2017 ).…”

Life-History Traits from Embryonic Development to Reproduction in the American Cockroach

“…Mated females lay their first ootheca approximately one day earlier than unmated females. The earlier oviposition of mated females may be related to mating behavior and male secretions such as sex peptides and sperm [ 50 , 51 ].…”

The Effects of Male Seminal Fluid Proteins on Gut/Gonad Interactions in Drosophila

“… Anatomical diagram of the organs and cell types of Drosophila melanogaster females that are involved in post-mating responses triggered by seminal proteins in the reproductive, digestive and nervous systems (not to scale). Figure elements are adapted from [ 33 , 34 , 35 ]. …”