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The brain-pituitary-gonadal axis of the three-spined stickleback, Gasterosteus aculeatus
Stockholm University, Faculty of Science, Department of Zoology.
2012 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The seasonal reproduction of the three-spined stickleback is stimulated by long day photoperiod. As in other vertebrates, the reproductive system of stickleback is regulated by the brain-pituitary-gonadal (BPG) axis which is largely controlled by feedback effects. Both negative and positive feedback effects on the BPG axis have been found in fish. So far, the roles feedback effects on the BPG axis play in the photoperiodic regulation of seasonal reproduction are still unclear. This thesis focused on the photoperiodic regulation and gonadal feedback effects on the gene expressions of gonadotropin (GtH) and gonadotropin-releasing hormones (GnRH) in the brain and pituitary, and how gonadal feedback regulated the steroid homeostasis in stickleback.Both GnRH2 and GnRH3 mRNA was found in the hypothalamus. Higher expression levels of both GnRH2 and 3 in breeding than in post-breeding males suggested that they are both involved in seasonal reproduction. There was no evidence for a role of GnRH3, which may be the dominating form, in the photoperiodic control of reproduction. However, the polarity of the feedback effect on gnrh3 gene expression may turn from positive to be negative when the males went into post-breeding state. Tapeworm, Schistocephalus solidus, infection inhibited the reproduction of sticklebacks. However, the infection caused higher expression levels of both GnRHs and GtHs genes, which may be due to feedback effect on the BPG axis.Under short day, both lh-β and fsh-β were suppressed by low androgen levels. This negative feedback may inhibit maturation completely, unless a rise of androgens triggers positive feedback under long day. The change in feedback polarity may result in all or nothing maturation. Furthermore, the androgen inhibitory effect on lh-β and fsh-β under short day could be abolished by aromatase inhibitor, which means the estrogen may cause negative feedback in males under short day.There was no compensation effect on plasma androgen level in fully mature hemi-castrated fish. However, both testosterone and 11-ketoandrostenedione treatments increased plasma levels much less in sham-operated fish than in castrated ones, indicating that homeostatic mechanisms are nevertheless present.

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University , 2012. , 39 p.
Keyword [en]
BPG axis, GnRH, lh-β, fsh-β, three-spined stickleback, Gasterosteus aculeatus, homeostasis, feedback
National Category
Zoology
Research subject
Functional Zoomorphology
Identifiers
URN: urn:nbn:se:su:diva-80473ISBN: 978-91-7447-568-5 (print)OAI: oai:DiVA.org:su-80473DiVA: diva2:555528
Public defence
2012-10-19, William-Olssonsalen, Geovetenskapens hus, Svante Arrhenius väg 14, Stockholm, 10:00 (English)
Opponent
Supervisors
Note

At the time of the doctoral defense, the following papers were unpublished and had a status as followsPaper 1: Submitted. Paper 3: Submitted. Paper 4: Submitted.

Available from: 2012-09-28 Created: 2012-09-20 Last updated: 2013-05-08Bibliographically approved
List of papers
1. GnRH mRNA levels in the brain of male three-spined stickleback, Gasterosteus aculeatus;effects of photoperiod, gonadectomy and breeding-postbreeding condition
Open this publication in new window or tab >>GnRH mRNA levels in the brain of male three-spined stickleback, Gasterosteus aculeatus;effects of photoperiod, gonadectomy and breeding-postbreeding condition
(English)Article in journal (Other academic) Submitted
Abstract [en]

In vertebrates, reproduction is regulated by the brain-pituitary-gonad (BPG) axis where thegonadotropin- releasing hormone (GnRH) is one of the components. However, very little isknown about the possible role of GnRHs in environmental and feedback control of fishreproduction. To investigate this, GnRH2 (chicken II GnRH) and GnRH3 (salmon GnRH) mRNAlevels in male three-spined stickleback (Gasterosteus aculeatus), where GnRH1 is absent,were measured in different reproductive conditions; breeding or post-breeding, treated withlong (LD: 16:8) or short (LD: 8:16) photoperiod and castrated or sham-operated in thebreeding season. Using in situ hybridization, specific GnRH3 RNA probe labeled cells wereobserved in hypothalamus and pituitary and ventral telecephalon, but barely in other brainareas. GnRH2 expressing cells were mainly located in the mesencephalon and thalamus, butwere found in hypothalamus and pituitary as well. The GnRH3 mRNA levels were always farhigher than GnRH2. Breeding male brains had considerably higher levels of both GnRH2 andGnRH3 mRNA than post-breeding male brains. This suggests that both forms havereproductive functions. Fish kept under long photoperiod, which stimulated breeding, hadhigher mRNA levels of GnRH2, but not of GnRH3 which is probably the hypophysiotropicform, than fish kept under non-stimulatory short photoperiod. Thus, the higher expressionsof gonadotropins under long than under short photoperiod are not likely to be regulated viaGnRHs. Furthermore, castrated males’ brains showed lower GnRH2 and GnRH3 mRNA levelsthan sham-operated ones. This is consistent with that the positive feedback known toregulate lh-β in this phase could be exerted via GnRHs.

Keyword
photoperiod, GnRH2, GnRH3, stickleback, feedback, mRNA
National Category
Zoology
Research subject
Zoological physiology
Identifiers
urn:nbn:se:su:diva-80873 (URN)
Available from: 2012-10-01 Created: 2012-10-01 Last updated: 2012-10-01Bibliographically approved
2. Schistocephalus solidus infections increase gonadotropins and gonadotropin releasing hormone (GnRH3) mRNA levels in the three-spined stickleback, Gasterosteus aculeatus
Open this publication in new window or tab >>Schistocephalus solidus infections increase gonadotropins and gonadotropin releasing hormone (GnRH3) mRNA levels in the three-spined stickleback, Gasterosteus aculeatus
Show others...
2012 (English)In: Parasitology international, ISSN 1383-5769, E-ISSN 1873-0329, Vol. 61, no 3, 470-474 p.Article in journal (Refereed) Published
Abstract [en]

Parasites often impair the reproduction of their hosts, one well known case being the cestode Schistocephalus solidus which is a common parasite in three-spined sticklebacks. Gasterosteus aculeatus. One of the possible ways that this could be exerted is by suppression on the brain-pituitary-gonadal (BPG) axis. In this study, mRNA levels of FSH-beta and LH-beta and of GnRH2 (cGnRH II) and GnRH3 (sGnRH) were measured via Q-PCR in infected and uninfected fish sampled from the field a few weeks before the onset of breeding. The pituitary mRNA levels of both FSH-beta and LH-beta were higher in infected males than in uninfected males. Also in females, FSH-beta mRNA levels were higher in infected individuals than in others, whereas there was no significant difference found in LH-beta expression. Brain mRNA levels of GnRH3 were higher in infected fish than in uninfected fish in both sexes, but no difference was found in GnRH2 mRNA levels. Thus, infection by S. solidus was able to alter the expressions not only of gonadotropins (GtHs), but also of GnRH which has not been observed previously. However, the effects are opposite to what should be expected if the parasite suppressed reproduction via actions on the brain-pituitary level. The gonads are perhaps more likely to be impaired by the parasites in other ways, and changed feedbacks on the BPG axis could then lead to the increases in GtHs and GnRH.

Keyword
Schistocephalus solidus, GnRH2, GnRH3, LH-beta, FSN-beta, Stickleback, mRNA
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-80632 (URN)10.1016/j.parint.2012.03.006 (DOI)000305501900014 ()
Note

AuthorCount:6;

Available from: 2012-09-25 Created: 2012-09-25 Last updated: 2017-11-06Bibliographically approved
3. Androgen feedback effects on LH and FSH, and photoperiodic control of reproduction in male three-spined sticklebacks, Gasterosteus aculeatus
Open this publication in new window or tab >>Androgen feedback effects on LH and FSH, and photoperiodic control of reproduction in male three-spined sticklebacks, Gasterosteus aculeatus
Show others...
2013 (English)In: General and Comparative Endocrinology, ISSN 0016-6480, E-ISSN 1095-6840, Vol. 182, 16-23 p.Article in journal (Refereed) Published
Abstract [en]

Sexual maturation in the stickleback is controlled by photoperiod. The aim of this study was to find out whether changes in feedback effects exerted by sex steroids could mediate the photoperiodic effect, which is regarded to be of an all-or-nothing character. To that end, males were castrated and treated with different doses of testosterone (T) and in one experiment also with the aromatase inhibitor fadrozole (AI) and kept under different photoperiods. In control fish, long day (LD 16:8) stimulated maturation, associated with more hypertrophied kidneys (a secondary sexual character) and higher levels of pituitary lhb and fshb mRNA than under short day conditions (LD 8:16). Under LD 8:16, low doses of T suppressed both lhb and fshb mRNA levels. However, with the use of high doses of T and/or longer photoperiods the inhibitory effects on lhb and fshb mRNA levels became less clear or instead positive effects were observed. Under intermediate photoperiod conditions, the negative feedback effect of a low dose of T on fshb was more prominent with shorter photoperiods, whereas no such shift was observed for lhb mRNA. The inhibitory effect of the low dose of T on lhb mRNA levels under LD 8:16 was abolished by AI, whereas the stimulatory effect of the high dose of T was not. The negative feedback effects were more marked under short days than under long days, whereas positive feedback effects were more marked under long days. The suppression of both fshb and lhb mRNA levels by low androgen levels, especially under short days, may inhibit maturation completely unless a rise of androgens above threshold levels would allow complete maturation.

Keyword
lhb, fshb, mRNA, Feedback, Reproduction, Stickleback, Photoperiod
National Category
Zoology
Research subject
Zoological physiology
Identifiers
urn:nbn:se:su:diva-88677 (URN)10.1016/j.ygcen.2012.10.017 (DOI)000315013100003 ()
Funder
Formas
Note

AuthorCount:6;

Available from: 2013-03-26 Created: 2013-03-25 Last updated: 2017-12-06Bibliographically approved
4. Homeostasis of circulating androgens levels in the male three-spined stickleback (Gasterosteus aculeatus)
Open this publication in new window or tab >>Homeostasis of circulating androgens levels in the male three-spined stickleback (Gasterosteus aculeatus)
2012 (English)In: Zoological Studies, ISSN 1021-5506, E-ISSN 1810-522X, Vol. 51, no 8, 1282-1289 p.Article in journal (Refereed) Published
Abstract [en]

In mammals, plasma androgen levels are regulated by homeostatic feedbackmechanisms operating in the brain-pituitary-gonadal axis. However, some earlierstudies suggest that this may not be the case in all teleosts. This study aims atinvestigating to what extent androgens levels are homeostatically regulated in malethree-spined stickleback (Gasterosteus aculeatus), and whether aromatisation ofandrogens plays a role in this. To that end, breeding male sticklebacks were eithercompletely castrated or hemi-castrated or sham-operated, and implanted with differentdoses of 11- ketoandrostenedione (11KA) and testosterone (T) or with the aromataseinhibitor (AI) fadrozole. Hemi-castration alone diminished androgen levels andcomplete castration almost removed them. Low doses of 11KA and T increasedplasma androgen levels in castrated but not in sham-operated fish. Both low and highdoses of 11KA increased plasma 11-ketotestosterone (11KT) in hemi-castrated fish,whereas only the high dose of 11KA did so in sham-operated fish. If aromatizationplays a role in homeostatic mechanisms, androgen levels would be expected to rise insham-operated fish treated with AI. However, this was not the case. The reduction ofplasma androgen levels in fully mature hemi-castrated fish may suggest that theremaining testis is not able to increase its steroidogenesis further. However, both311KA and T treatments increased plasma levels much less in sham-operated fish thanin castrated ones, indicating that homeostatic mechanisms are nevertheless present.

Keyword
steroid, RIA, homeostasis, feedback, stickleback
National Category
Zoology
Research subject
Zoological physiology
Identifiers
urn:nbn:se:su:diva-80875 (URN)
Available from: 2012-10-01 Created: 2012-10-01 Last updated: 2017-12-07Bibliographically approved

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