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Overripening of eggs and changes in reproductive hormones in the threespine stickleback, Gasterosteus aculeatus
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0003-0022-0698
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Number of Authors: 8
2016 (English)In: Evolutionary Ecology Research, ISSN 1522-0613, E-ISSN 1937-3791, Vol. 17, no 3, 583-601 p.Article in journal (Refereed) Published
Abstract [en]

Background: Female threespine sticklebacks, Gasterosteus aculeatus, are batch spawners. As in most teleosts, the ovulated eggs are kept in the ovarian cavity until spawning. If spawning or spontaneous release of the eggs does not take place, they can become overripe and harden, and in most cases remain in the ovary. The overripe eggs are lost for reproduction and also block further spawnings. Reproductive hormones regulate egg production and may be involved in the mechanism of overripening. Question: What are the reproductive endocrinological parameters characterizing overripening of ovulated eggs in the threespine stickleback? Organism: Wild-caught adult threespine sticklebacks from the southern Baltic at Skare in southern Sweden and the island of Asko in northwestern Baltic Proper in Sweden. Experiments: We collected blood samples for hormone measurements, as well as pituitaries and brains for measurement of mRNA from both sexually mature non-overripe (non-ovulated and/or ovulated) and overripe (egg-bound) females. For the Skare fish, sexual maturation was induced under laboratory conditions by exposure to a long photoperiod and we compared the non-overripe (including non-ovulated, with oocytes in different maturing or ripening stages, and ovulated females) with the overripe females. The Asko fish were sampled directly from nature, during the natural summer breeding season and we compared the non-overripe (including non-ovulated, with oocytes in different maturing or ripening stages, and ovulated females) with the overripe females. Methods: In the fish collected from Skare, we used radioimmunoassay to measure the plasma levels of four steroids: testosterone, estradiol, 17,20 beta-dihydroxypregn-4-en-3-one (17,20 beta-P), and 17,20 beta, 21-trihydroxypregn-4-en-3-one (17,20 beta,21-P). We also measured the mRNA levels of gonadotropins [GTHs: follicle-stimulating hormone (fsh-beta) and luteinizing hormone (lh-beta)] in the pituitary, and of gonadotropin-releasing hormones (GnRHs: gnrh2, gnrh3) and kisspeptin (kiss2) and its G protein-coupled receptor (gpr54) in the brain by real-time quantitative PCR. In the fish collected from Asko, we measured only progestogens (17,20 beta-P and 17,20 beta,21-P). Results: In the fish from Skare, overripe female sticklebacks had significantly lower levels of circulating plasma steroid hormones (testosterone, estradiol, 17,20 beta-P), as well as of pituitary lh-beta and brain kiss2 and gpr54 mRNA than the non-overripe females. In the fish caught from Asko, overripe females had lower 17,20 beta-P levels than the non-overripe non-ovulated females, but there was no difference between the non-overripe ovulated and the overripe females. The 17,20 beta,21-P plasma levels were under the limit of detection in all groups.

Place, publisher, year, edition, pages
2016. Vol. 17, no 3, 583-601 p.
Keyword [en]
testosterone, estradiol, 17, 20 beta-dihydroxypregn-4-en-3-one, 17, 20 beta, 21-trihydroxypregn-4-en-3-one, fsh-beta, lh-beta, gnrh2, gnrh3, kiss2, gpr54, ovulation, spawning, overripe, reproduction, stickleback, teleosts
National Category
Zoology
Research subject
Functional Zoomorphology
Identifiers
URN: urn:nbn:se:su:diva-132565ISI: 000378168800008OAI: oai:DiVA.org:su-132565DiVA: diva2:953599
Available from: 2016-08-18 Created: 2016-08-15 Last updated: 2017-06-01Bibliographically approved
In thesis
1. Reproductive physiology of the female three-spined stickleback, Gasterosteus aculeatus
Open this publication in new window or tab >>Reproductive physiology of the female three-spined stickleback, Gasterosteus aculeatus
2017 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Reproduction in vertebrates, including fishes, is under control of the brain-pituitary-gonad (BPG) axis. The female three-spined stickleback, Gasterosteus aculeatus, produces egg clutches at intervals of a few days and spawns them in a nest built by male. Following ovulation, eggs are stored in the ovarian cavity surrounded by the ovarian fluid (OF). If spawning or spontaneous release do not occur, the eggs can undergo overripening, a phenomenon occurring both in nature and captivity.

In this PhD thesis, the changes of reproductive hormones and vitellogenesis were studied at overripening of eggs and over the natural spawning cycle. OF properties were also examined at overripening of eggs and after treatment with sex steroids.

Plasma levels of steroids: testosterone (T), estradiol (E2), 17,20β-dihydroxypregn-4-en-3-one (17,20β-P) and 17,20β,21-trihydroxypregn-4-en-3-one (17,20β,21-P) were measured by radioimmunoassay, and relative mRNA levels of the pituitary gonadotropins (fsh-β/lh-β), brain gonadotropin-releasing hormones (gnrh2/gnrh3) and kisspeptin and its receptor (kiss2/gpr54) by qPCR. Overripening of eggs was accompanied with a significant reduction in most of endocrine parameters of BPG axis (T, E2, 17,20β-P; lh-β; kiss2, gpr54). Low level of hormones could be advantageous for the overripe egg-bound females, since this would reduce further ovulations giving higher chances to survive and reproduce again. Over the 3-day spawning cycle, T and E2 were highly correlated, showed cyclicity with low levels at ovulation and increasing from 24 and 6 hours post-spawning (hps), respectively. Spawning may give rise to this increase as these rises did not occur if release of the eggs does not happen (overripe females). A peak at pituitary lh-β mRNA levels appeared 48 hps, a day before the next ovulation. No significant changes were found for the other studied hormones.

Vitellogenesis was studied by measurement of the vitellogenin mRNA levels in the liver by qPCR. The levels were highest at 24 and 48 hps and were positively correlated to both E2 and T over the cycle. However, changes were small suggesting a rather continuous vitellogenesis over the stickleback spawning cycle which could be an advantage for a multiple spawner with a limited spawning season. Overripening reduced vitellogenin mRNA levels but did not abolish it.

OF amount was diminished in overripe females and had a lower viscocity but higher dry weight and protein levels than in non-overripe ovulated females, suggesting that changes in OF properties are related to the egg overripening. The effects of steroids were studied using Silastic capsules. T and 17,20β-P induced an increase of OF amount, but protein levels were only increased in 17,20β-P-treated females, proposing a role of this steroid in the control of OF secretion. 1-D SDS-PAGE showed that OF contained several proteins, some of them came from eggs, but no consistent differences between groups.

Concluding, the knowledge of the reproductive physiological changes is important for understanding their essential roles in the production of viable eggs in this species but also in the reproductive physiology of female fishes in general.

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University, 2017. 65 p.
Keyword
overripening of eggs, spawning cycle, brain-pituitary-gonad (BPG) axis, vitellogenin, ovarian fluid, sex steroids, reproduction, three-spined stickleback, Gasterosteus aculeatus, fish
National Category
Biological Sciences Zoology Other Biological Topics
Research subject
Functional Zoomorphology
Identifiers
urn:nbn:se:su:diva-143279 (URN)978-91-7649-854-5 (ISBN)978-91-7649-855-2 (ISBN)
Public defence
2017-09-08, Vivi Täckholmsalen (Q-salen), NPQ-huset, Svante Arrhenius väg 20, Stockholm, 13:00 (English)
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Note

At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 3: Manuscript. Paper 4: Manuscript.

Available from: 2017-08-16 Created: 2017-05-22 Last updated: 2017-08-14Bibliographically approved

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