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The juvenile three-spined stickleback: model organism for the study of estrogenic and androgenic endocrine disruption in laboratory and field
Stockholm University, Faculty of Science, Department of Systems Ecology.
2004 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Industrial and domestic sewage effluents have been found to cause reproductive disorders in wild fish, often as a result of the interference of compounds in the effluents with the endocrine system. This thesis describes laboratory-based exposure experiments and a field survey that were conducted with juveniles of the three-spined stickleback, Gasterosteus aculeatus. This small teleost is a common fish in Swedish coastal waters and was chosen as an alternative to non-native test species commonly used in endocrine disruption studies, which allows the comparison of field data with results from laboratory experiments.

The aim of this thesis was to elucidate 1) if genetic sex determination and differentiation can be disturbed by natural and synthetic steroid hormones and 2) whether this provides an endpoint for the detection of endocrine disruption, 3) to evaluate the applicability of specific estrogen- and androgen-inducible marker proteins in juvenile three-spined sticklebacks, 4) to investigate whether estrogenic and/or androgenic endocrine disrupting activity can be detected in effluents from Swedish pulp mills and domestic sewage treatment plants and 5) whether such activity can be detected in coastal waters receiving these effluents.

Laboratory exposure experiments found juvenile three-spined sticklebacks to be sensitive to water-borne estrogenic and androgenic steroid substances. Intersex – the co-occurrence of ovarian and testicular tissue in gonads – was induced by 17β-estradiol (E2), 17α-ethinylestradiol (EE2), 17α-methyltestosterone (MT) and 5α-dihydrotestosterone (DHT). The first two weeks after hatching was the phase of highest sensitivity. MT was ambivalent by simultaneously eliciting masculinizing and feminizing effects. When applying a DNA-based method for genetic sex identification, it was found that application of MT only during the first two weeks after hatching caused total and apparently irreversible development of testis in genetic females. E2 caused gonad type reversal from male to female. E2 and EE2 induced vitellogenin - the estrogen-responsive yolk precursor protein, while DHT and MT induced spiggin – the androgen-responsive glue protein of the stickleback.

None of the effluents from two pulp mills and two domestic sewage treatment plants had any estrogenic or androgenic activity. Juvenile three-spined sticklebacks were collected during four subsequent summers at the Swedish Baltic Sea coast in recipients of effluents from pulp mills and a domestic sewage treatment plant as well as remote reference sites. No sings of endocrine disruption were observed at any site, when studying gonad development or marker proteins, except for a deviation of sex ratios at a reference site.

The three-spined stickleback – with focus on the juvenile stage – was found to be a sensitive species suitable for the study of estrogenic and androgenic endocrine disruption.

Place, publisher, year, edition, pages
Stockholm: Institutionen för systemekologi , 2004. , 40 p.
Keyword [en]
endocrine disruption
National Category
Ecology
Identifiers
URN: urn:nbn:se:su:diva-296ISBN: 91-7265-976-9 (print)OAI: oai:DiVA.org:su-296DiVA: diva2:192101
Public defence
2004-12-10, William-Olssonsalen, Geovetenskapens hus, Svante Arrhenius väg 8 A, Stockholm, 10:00
Opponent
Supervisors
Available from: 2004-11-18 Created: 2004-11-18Bibliographically approved
List of papers
1. The juvenile three-spined stickleback (Gasterosteus aculeatus L.) as a model organism for endocrine disruption I: Sexual differentiation
Open this publication in new window or tab >>The juvenile three-spined stickleback (Gasterosteus aculeatus L.) as a model organism for endocrine disruption I: Sexual differentiation
2004 (English)In: Aquatic Toxicology, ISSN 0166-445X, E-ISSN 1879-1514, Vol. 70, no 4, 287-310 p.Article in journal (Refereed) Published
Abstract [en]

Juvenile three-spined stickleback (Gasterosteus aculeatus L.) is introduced as a unique model organism for both androgenic and oestrogenic endocrine action. Intersex is often used as an indicator for disruption of sexual differentiation in fish exposed to different kinds of effluents from human activities. In wild fish it has exclusively been reported in terms of feminisation due to xenoestrogens in the environment. The assumption that the intersex individuals are feminised genetic males can only be proven by genetic sex identification of the intersexual individuals. Intersex and gonadal sex reversal were induced in three-spined sticklebacks by treatment with natural and synthetic steroid hormones. Juvenile sticklebacks were exposed to three nominal concentrations of 17β-oestradiol (E2); i.e. 0.01, 1.0 and 10.0 μg/L; which were administered to the water either continuously from hatching to the end of the experiment (39–58 days post hatch), during the first 2 weeks after hatching only, from 14 days after hatching onwards, or during the chorionated embryo stage until hatching. Other groups were exposed to 17α-ethinylestradiol (EE2) at 0.05 μg/L and 17α-methyltestosterone (MT) at 1.0 μg/L (nominal concentrations). MT was applied continuously, during the first 2 weeks post hatch only, or from 14 days after hatching onwards. Gonad histology was examined and the genetic sex was identified with male sex-linked PCR markers. Treatment with oestrogens caused feminisation at the two highest E2 concentrations and with EE2. Exposure to E2 before hatching had no effect. Intersexual individuals from oestrogen treatments were genetic males. The genetic sex marker identified apparent total reversal of the gonad type of genetic males. Treatment with MT did not reveal a clear picture, since intersex was observed in both genetic females and males. MT also caused severe testis abnormalities, mainly the development of large branched cavities with unidentified origin. The process of sex differentiation is most sensitive to the influence of external steroids during the first 2 weeks after hatching. A lower incidence of intersex could also be induced in sticklebacks exposed from 14 days after hatching by E2 treatment, but not with MT. The combination of gonad histopathology with genetic sex identification in juvenile sticklebacks is suggested as a tool for detecting endocrine disruption in laboratory studies, and might become very useful in field surveys.

Keyword
Gasterosteus aculeatus, Stickleback, Sex differentiation, Sex steroids, Intersex, Endocrine disruption
National Category
Natural Sciences
Identifiers
urn:nbn:se:su:diva-23435 (URN)10.1016/j.aquatox.2004.10.003 (DOI)
Available from: 2004-11-18 Created: 2004-11-18 Last updated: 2017-12-13Bibliographically approved
2. The juvenile three-spined stickleback (Gasterosteus aculeatus L.) as a model organism for endocrine disruption II: kidney hypertrophy, vitellogenin and spiggin induction
Open this publication in new window or tab >>The juvenile three-spined stickleback (Gasterosteus aculeatus L.) as a model organism for endocrine disruption II: kidney hypertrophy, vitellogenin and spiggin induction
Show others...
2004 (English)In: Aquatic Toxicology, ISSN 0166-445X, E-ISSN 1879-1514, Vol. 70, no 4, 311-326 p.Article in journal (Refereed) Published
Abstract [en]

This study investigated the suitability of juvenile three-spined sticklebacks, Gasterosteus aculeatus L., for detecting both androgen- and oestrogen-induced endocrine disruption. The investigated endpoints were kidney hypertrophy and the induction of the protein markers spiggin and vitellogenin. Juveniles were exposed to steroid hormones 17β-oestradiol (E2: nominal 0.01, 1.0 and 10 μg/L), 17α-ethinylestradiol (EE2: nominal 0.05 μg/L) and 17α-methyltestosterone (MT: nominal 1.0 μg/L) from the day of hatching until the termination of the experiments between 39 and 58 days after hatching. E2 (10 μg/L) and MT were applied during different time windows: (a) 14 days after hatching only and (b) continuously with start 14 days after hatching.

Kidney hypertrophy is an androgen-dependent secondary sexual character in adult male sticklebacks and corresponds to the production of the glue protein spiggin during the breeding season. The kidneys were hypertrophied and spiggin levels were elevated in juvenile sticklebacks after treatment with MT. Paradoxically, slightly elevated spiggin levels and kidney hypertrophy were observed also in fish treated with high dose E2. Levels of vitellogenin, the oestrogen-inducible yolk precursor protein, were elevated in juvenile sticklebacks after E2 medium and high dose and EE2 treatment.

The tested endpoints are suitable for the study of endocrine disruption in juvenile sticklebacks, a fish species that is easy to handle in laboratory and relevant for temperate geographical regions.

Place, publisher, year, edition, pages
Elsevier B.V., 2004
Keyword
Gasterosteus aculeatus; Stickleback; Sex steroids; Vitellogenin; Spiggin; Endocrine disruption
National Category
Earth and Related Environmental Sciences
Identifiers
urn:nbn:se:su:diva-23436 (URN)10.1016/j.aquatox.2004.10.004 (DOI)
Note
Part of urn:nbn:se:su:diva-296Available from: 2004-11-18 Created: 2004-11-18 Last updated: 2017-12-13Bibliographically approved
3. The application of DNA sex identification to evaluate intersexuality and to verify gonad type reversal in juvenile three-spined stickleback (Gasterosteus aculeatus)
Open this publication in new window or tab >>The application of DNA sex identification to evaluate intersexuality and to verify gonad type reversal in juvenile three-spined stickleback (Gasterosteus aculeatus)
Article in journal (Refereed) Submitted
Identifiers
urn:nbn:se:su:diva-23437 (URN)
Note
Part of urn:nbn:se:su:diva-296Available from: 2004-11-18 Created: 2004-11-18Bibliographically approved
4. Monitoring androgenic and estrogenic endocrine disruption in sewage and pulp mill effluents and in coastal waters in Sweden with the juvenile three-spined stickleback (Gasterosteus aculeatus)
Open this publication in new window or tab >>Monitoring androgenic and estrogenic endocrine disruption in sewage and pulp mill effluents and in coastal waters in Sweden with the juvenile three-spined stickleback (Gasterosteus aculeatus)
Show others...
Manuscript (Other academic)
Identifiers
urn:nbn:se:su:diva-23438 (URN)
Note
Part of urn:nbn:se:su:diva-296Available from: 2004-11-18 Created: 2004-11-18 Last updated: 2010-01-13Bibliographically approved

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