High levels of circulating prostaglandin F associated with ovulation stimulate female sexual receptivity and spawning behavior in the goldfish (Carassius auratus)

Peter W. Sorensen, Christopher Appelt, Norman E. Stacey, Fredrick Wm Goetz, Alan R. Brash

Research output: Contribution to journalArticlepeer-review

9 Scopus citations

Abstract

This study tested the hypothesis that blood-borne prostaglandin F (PGF) produced at the time of ovulation by female goldfish, a typical scramble-spawning, egg-laying cyprinid fish, functions as a hormone which stimulates female sexual receptivity, behavior, and pheromone release, thereby synchronizing female mating behavior with egg availability. We conducted 5 experiments. First, we tested whether PGF is found in the blood of female fish and if it increases at the time of ovulation. Using gas chromatography–mass spectrometry, we found that circulating PGF was approximately 1 ng/ml prior to ovulation, increased over 50-fold within 3 h of ovulation and returned to preovulatory values after spawning and egg release. Ovulated fish also released over 2 ng/h of PGF and 800 ng/h of 15-keto-PGF, a metabolite of PGF – both compounds with known pheromonal function. Second, we tested how closely levels of circulating PGF tracked the timing of ovulation by sampling fish at the time of ovulation and discovered that PGF increased within 15 min of ovulation, peaked after 9 h, and fell to basal levels as fish spawned and released their eggs. Third, we tested whether an interaction between eggs and the reproductive tract serves as a source of circulating PGF and its relationship with female sexual receptivity by injecting ovulated eggs (or an egg-substitute) into the reproductive tract of females stripped of ovulated eggs. We found both of these treatments elicited measurable increases in plasma PGF as well as female sexual behavior. A fourth experiment showed that indothemacin, a PG synthase inhibitor, blocked both PGF increase and female sexual behavior in egg-substitute-injected fish. Finally, we tested the relationship between the expression of female behavior and PGF in PGF-injected fish and found that circulating PGF levels closely paralleled behavior, rising within 15 min and peaking at 45 min. Together, these experiments establish that PGF functions as a behavioral blood-borne hormone in the goldfish, suggesting it likely has similar activity in other related, externally-fertilizing fishes.

Original languageEnglish (US)
Pages (from-to)128-136
Number of pages9
JournalGeneral and Comparative Endocrinology
Volume267
DOIs
StatePublished - Oct 1 2018

Bibliographical note

Funding Information:
We thank Linda Bowdin for help with the immunoassays, William Boeglin for helping with GC-MS, Ron Kellner and Lance Vreize for help with behavioral observation. We thank two anonymous reviewers for their helpful comments. This study was funded by the National Science Foundation (BNS9109027; BNS 9723798) (PWS), the Minnesota Agricultural Experiment Station (PWS), and the National Institutes of Health (Prostaglandin Core Laboratory; Grant # HD05797; ARB).

Publisher Copyright:
© 2018

Copyright:
Copyright 2018 Elsevier B.V., All rights reserved.

Keywords

  • Behavior
  • Hormone
  • Ovulation
  • Pheromone
  • Prostaglandin

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