Drosophila melanogaster sex peptide regulates mated female midgut morphology and physiology

Proc Natl Acad Sci U S A. 2021 Jan 5;118(1):e2018112118. doi: 10.1073/pnas.2018112118.

Abstract

Drosophila melanogaster females experience a large shift in energy homeostasis after mating to compensate for nutrient investment in egg production. To cope with this change in metabolism, mated females undergo widespread physiological and behavioral changes, including increased food intake and altered digestive processes. The mechanisms by which the female digestive system responds to mating remain poorly characterized. Here, we demonstrate that the seminal fluid protein Sex Peptide (SP) is a key modulator of female post-mating midgut growth and gene expression. SP is both necessary and sufficient to trigger post-mating midgut growth in females under normal nutrient conditions, and likely acting via its receptor, Sex Peptide Receptor (SPR). Moreover, SP is responsible for almost the totality of midgut transcriptomic changes following mating, including up-regulation of protein and lipid metabolism genes and down-regulation of carbohydrate metabolism genes. These changes in metabolism may help supply the female with the nutrients required to sustain egg production. Thus, we report a role for SP in altering female physiology to enhance reproductive output: Namely, SP triggers the switch from virgin to mated midgut state.

Keywords: Drosophila post-mating response; digestive tract; gut growth; sex peptide; transcriptome.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Copulation
  • Digestive System / anatomy & histology
  • Digestive System / growth & development
  • Digestive System / metabolism*
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / metabolism*
  • Female
  • Fertility / genetics
  • Fertility / physiology*
  • Gene Ontology
  • Intercellular Signaling Peptides and Proteins / metabolism*
  • Intestines / anatomy & histology
  • Intestines / growth & development
  • Intestines / physiology
  • Male
  • Receptors, Peptide / genetics
  • Receptors, Peptide / metabolism*
  • Reproduction / genetics
  • Reproduction / physiology*
  • Semen / metabolism
  • Sexual Behavior, Animal / physiology
  • Transcriptome / genetics*
  • Transcriptome / physiology

Substances

  • Drosophila Proteins
  • Intercellular Signaling Peptides and Proteins
  • Receptors, Peptide
  • male accessory gland peptide, Drosophila
  • sex peptide receptor, Drosophila