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Developmental exposure of zebrafish (Danio rerio) to 17α-Ethinylestradiol affects non-reproductive behavior and fertility as adults, and increases anxiety in unexposed progeny
Södertörns högskola, Institutionen för naturvetenskap, miljö och teknik, Biologi. Örebro University.
Södertörns högskola, Institutionen för naturvetenskap, miljö och teknik, Biologi. Örebro University.
Södertörns högskola, Institutionen för naturvetenskap, miljö och teknik, Miljövetenskap.ORCID-id: 0000-0001-7239-7121
Södertörns högskola, Institutionen för naturvetenskap, miljö och teknik, Biologi.
Vise andre og tillknytning
2015 (engelsk)Inngår i: Hormones and Behavior, ISSN 0018-506X, E-ISSN 1095-6867, Vol. 73, s. 30-38Artikkel i tidsskrift (Fagfellevurdert) Published
Abstract [en]

Exposure to estrogenic endocrine disruptors (EDCs) during of development affects fertility, reproductive and non-reproductive behavior in mammals and fish. These effects can also be transferred to coming generations. In fish, the effects of developmental EDC exposure on non-reproductive behavior is less well studied. Here, we analyze the effects of 17α-Ethinylestradiol (EE2) on anxiety, shoaling behavior and fertility in zebrafish after developmental treatment and remediation in clean water until adulthood. Zebrafish embryos were exposed from day 1 to day 80 post fertilization to actual concentrations of 1.2 and 1.6ng/L EE2. After remediation for 82days non-reproductive behavior and fertilization success were analyzed in both sexes. Males and females from the 1.2ng/L group, as well as control males and females, were bred, and behavior of the untreated F1 offspring was tested as adults. Developmental treatment with 1.2 and 1.6ng/L EE2 significantly increased anxiety in the Novel Tank test and increased shoaling intensity in both sexes. Fertilization success was significantly reduced by EE2 in both sexes when mated with untreated fish of opposite sex. Progeny of fish treated with 1.2ng/L EE2 showed increased anxiety in the Novel tank test and increased light avoidance in the Scototaxis test compared to control offspring. In conclusion, developmental exposure of zebrafish to low doses of EE2 resulted in persistent changes in behavior and fertility. The behavior of unexposed progeny were affected by their parents' exposure, which might suggest transgenerational effects.

sted, utgiver, år, opplag, sider
Academic Press, 2015. Vol. 73, s. 30-38
Emneord [en]
17α-Ethinylestradiol; Anxiety; Developmental exposure; Endocrine disruptors; F1 effects; Fertility; Neuroendocrinology; Social behavior; Stress behavior; Zebrafish
HSV kategori
Forskningsprogram
Miljövetenskapliga studier; Östersjö- och Östeuropaforskning
Identifikatorer
URN: urn:nbn:se:sh:diva-27795DOI: 10.1016/j.yhbeh.2015.05.014ISI: 000360251800005PubMedID: 26072466Scopus ID: 2-s2.0-84934983120Lokal ID: 1556/42/2011OAI: oai:DiVA.org:sh-27795DiVA, id: diva2:823634
Ingår i projekt
Endocrine disruption in fish: Effects on behaviour and reproduction, development af biomarkers and assessment of risk levels in the Baltic Sea, The Foundation for Baltic and East European StudiesEndocrine disruption in fish: Risk identification, development of biomarkers and assessment of risk levels in the Baltic Sea, The Foundation for Baltic and East European Studies
Forskningsfinansiär
The Foundation for Baltic and East European Studies, A037-2008The Foundation for Baltic and East European Studies, A065-2011Tilgjengelig fra: 2015-06-18 Laget: 2015-06-18 Sist oppdatert: 2020-07-17bibliografisk kontrollert
Inngår i avhandling
1. Fishy behavior: persistent effects of early-life exposure to 17α-ethinylestradiol
Åpne denne publikasjonen i ny fane eller vindu >>Fishy behavior: persistent effects of early-life exposure to 17α-ethinylestradiol
2015 (engelsk)Doktoravhandling, med artikler (Annet vitenskapelig)
Abstract [en]

The synthetic estrogen 17α-ethinylestradiol (EE2) is an endocrine disrupting chemical (EDC) of concern due to its persistent nature and widespread presence in the aquatic environment. In mammals, effects of developmental EDC exposure on reproduction and behavior not only persist to adulthood after discontinued exposure, but are also inherited by several consecutive unexposed generations. The results presented in this thesis demonstrate that non-reproductive behavior in fish is highly sensitive to the influence of EE2 during development and the effects do not appear to be restored after a long recovery period in clean water. We have shown that exposure to low doses of EE2 during development results in increased anxiety in two fish species (zebrafish and guppy) and their offspring. We have also demonstrated that the effects of EE2 on anxiety are apparent in both sexes and are transgenerationally transmitted to two consecutive generations of unexposed offspring in the guppy. In order to investigate the possible biological mechanisms of the observed persistent effects on non-reproductive behavior, we also performed an RNA sequencing analysis of the whole-brain transcriptome in developmentally exposed zebrafish after remediation in clean water until adulthood. Differential expression of 33 genes in males and 62 genes in females were observed as a result of EE2 exposure, with only one gene affected in both sexes. Functional analysis revealed cholesterol biosynthesis and circadian rhythm to be the top two affected pathways in males and females, respectively. Both pathways have previously been implicated in anxiety behavior and represent possible candidates connecting the transcriptome alterations to the observed behavioral phenotype. The study represents an initial survey of the fish brain transcriptome by means of RNA sequencing after long-term recovery from developmental exposure to an estrogenic compound.

sted, utgiver, år, opplag, sider
Örebro: Örebro university, 2015. s. 62
Serie
Örebro Studies in Biology, ISSN 1650-8793 ; 9Södertörn doctoral dissertations, ISSN 1652-7399 ; 110
Emneord
Endocrine disruptors, anxiety, stress behavior, transgenerational effects, 17α-ethinylestradiol, developmental exposure, social behavior, fish
HSV kategori
Forskningsprogram
Biologi
Identifikatorer
urn:nbn:se:sh:diva-28426 (URN)978-91-7529-091-1 (ISBN)
Disputas
2015-10-05, Hörsalen, Musikhögskolan, Örebro, 13:00 (engelsk)
Opponent
Veileder
Tilgjengelig fra: 2015-10-01 Laget: 2015-10-01 Sist oppdatert: 2015-10-01bibliografisk kontrollert
2. Hitting the mark: Studies of alterations in behaviour and fertility in ethinyl estradiol-exposed zebrafish and search related biomarkers
Åpne denne publikasjonen i ny fane eller vindu >>Hitting the mark: Studies of alterations in behaviour and fertility in ethinyl estradiol-exposed zebrafish and search related biomarkers
2016 (engelsk)Doktoravhandling, med artikler (Annet vitenskapelig)
Abstract [en]

In this thesis, we have analysed the effects of EE2 on non-reproductive behaviours and fertility. We have showed that two doses of EE2 in male adult short-term exposures evokes opposite behaviours in the novel tank test. A lower dose induced increased bottom-dwelling, a sign of increased anxiety and a higher dose increased surface-dwelling, which would likely expose themselves to predation in a natural environment. Increased shoaling was observed in both exposures, possibly affecting feeding and reproduction opportunities. Fertility analysis of these fish demonstrated a complete inhibition of spawning in the highest dose group. To investigate mechanisms behind the spawning failure, we examined expression levels of genes involved in zebrafish sex differentiation and maintenance of gonadal function. We found downregulated transcription levels of male-predominant genes, suggesting a demasculinization of the testes contributing to functional sterility in these fish. We have demonstrated that non-reproductive behaviour in zebrafish is highly sensitive to EE2 exposure during development. After exposing male and female zebrafish to low doses of EE2 followed by remediation in clean water until adulthood, the fish displayed increased anxiety and shoaling behaviour, demonstrating persistent effects of EE2. Furthermore, behavioural effects were transferred to their progeny. Decreased fertilisation success of the developmentally exposed fish was observed in both sexes when mated to untreated animals of the opposite sex. These fertility effects persisted although the fish had a long remediation period, implying likely reduced fitness of fish populations in aquatic environments. Based on our findings on non-reproductive behaviours and fertility, we performed RNAsequencing analysis of the brain and testes in order to investigate possible biological mechanisms behind the persistent effects. There is a need for biomarkers allowing detection of both reversible and irreversible effects in animals exposed to estrogenic substances, hopefully contributing to better risk assessments for EDCs. Results from RNA-sequencing would serve as a basis for continued studies in pursuit of potential biomarkers.

sted, utgiver, år, opplag, sider
Örebro: Örebro university, 2016. s. 55
Serie
Örebro Studies in Biology, ISSN 1650-8793 ; 10Södertörn doctoral dissertations, ISSN 1652-7399 ; 115
Emneord
Endocrine disrupting compounds, 17α-ethinylestradiol, fertility, anxiety, behaviour, zebrafish, biomarkers, stress
HSV kategori
Identifikatorer
urn:nbn:se:sh:diva-29440 (URN)978-91-7529-115-4 (ISBN)
Disputas
2016-02-25, Sal MA636, Alfred Nobels allé 7, Huddinge, 13:00 (engelsk)
Opponent
Veileder
Forskningsfinansiär
The Foundation for Baltic and East European Studies
Tilgjengelig fra: 2016-02-04 Laget: 2016-02-04 Sist oppdatert: 2016-02-04bibliografisk kontrollert
3. Endocrine disruption in fish: Effects of 17α-ethinylestradiol exposure on non-reproductive behavior, fertility and brain and testis transcriptome
Åpne denne publikasjonen i ny fane eller vindu >>Endocrine disruption in fish: Effects of 17α-ethinylestradiol exposure on non-reproductive behavior, fertility and brain and testis transcriptome
2018 (engelsk)Doktoravhandling, med artikler (Annet vitenskapelig)
Abstract [en]

Aquatic environments are the end recipient for most anthropogenic chemical pollutants. One common chemical pollutant found in the aquatic environment is 17α-ethinylestradiol (EE2), a synthetic estrogen used in contraceptive pills. EE2 is found in sewage treatment plant effluents and surface waters in concentrations from non-detectable up to 300 ng/L. EE2 has the ability to bioaccumulate and is more than 10 fold more potent in fish than the natural counterpart estradiol. Exposure has led to skewed sex ratios, decreased egg and sperm production, and altered reproductive behavior.  The aim of this thesis was to investigate the effects of EE2 exposure on non-reproductive behavior and fertility in fish. We found that zebra fish exposed to low concentrations of EE2 during development showed increased anxiety-like behavior and decreased fertility that were persistent in adulthood, even after a long remediation period in clean water. The altered behavior and lowered fertility were accompanied by alterations in the testis and brain transcriptome of possible significance for the behavior and fertility effects. The zebrafish was also used in adult exposures of EE2 and citalopram, alone and in combination to investigate if behavioral effects can be detected at very low concentrations, and if so, if the two compounds would interact and affect the behavioral outcome. Anxiety-like behavior was altered by EE2 and the two compounds in combination affected the outcome of each other. Further, when developmental exposure of progeny to wild caught three spined stickleback was used as a link between laboratory fish and natural fish populations, EE2 was found to decrease the anxiety-like behavior in the adult stickleback as well as cause ovotestis and intersex, feminization and sex reversal of genetic males. In conclusion, fertility and non-reproductive behaviors in the zebrafish and three spined stickleback are sensitive to EE2 exposure and effects from developmental exposures seem to be persistent.  Fertility and behavior are of high ecological significance for fish and alterations due to EE2 exposure might have negative effects on population fitness. The persistent alterations in the transcriptome of the zebrafish testis and brain lead to generation of hypotheses of mechanisms involved in the behavior and reproductive phenotypes caused by developmental exposure to EE2.

Abstract [sv]

Den akvatiska miljön är ofta särskilt utsatt för miljöföroreningar då de flesta ämnen förr eller senare sprids dit genom bland annat markavrinning, nedfall från luften och/eller från vattenreningsverk. Syntetiskt östrogen som används i p-piller, 17α-etinylestradiol (EE2), sprider sig ofta till vattenmiljön från avloppsvatten, då det bara delvis renas bort i vattenreningsprocessen. EE2 är ett hormonstörande ämne med förmågan att ansamlas i organismer och mer än tio gånger så verksamt i fisk som det naturliga hormonet estradiol (E2). Man har tidigare sett att exponering för EE2 även i de låga halter som påvisas vid vattenreningsverk bland annat har lett till minskade produktion av ägg och spermier samt förändrade parningsbeteenden.

I denna avhandling undersöks effekterna av EE2 på fiskars icke-reproduktiva beteende och fertilitet. Dessa faktorer är av hög ekologisk relevans för fisk då förändringar på dessa kan ge negativa effekter på populationsnivå. Resultaten visar att zebrafisk som exponeras för låga halter av EE2 under utvecklingen uppvisar ett mer ängsligt beteende och har lägre fertilitet när de blir vuxna även efter en lång återhämtningsperiod i rent vatten. Det förändrade beteendet uppvisas även hos avkomman till dessa fiskar.  Förändringarna i beteende och fertilitet åtföljdes av förändringar i hjärnans och testikelvävnadens transkriptom, dvs. förändringar i vilka gener som uttrycks. I zebrafiskens testikelvävnad hittades bland annat en skillnad i uttryck av gener kopplade till könsdifferentiering och utveckling samt spermatogenesen, gener som kan ha betydelse för den nedsatta fertiliteten. I zebrafiskens hjärna hittades ingen skillnad i uttryck på gener direkt kopplade till stressaxeln men däremot på flera andra gener i nätverk som indirekt kan kopplas till det ängsliga beteendet som dygnsrytm och kolesterolsyntes. I naturen exponeras organismer ofta för en blandning av föroreningar. Därför undersöktes också effekter av EE2 i kombination med citalopram, ett antidepressivt läkemedel som ofta påvisas i vattenmiljön, för att undersöka om förändringar i beteende kan påvisas även vid väldigt låga koncentrationer av varje ämne och, om så är fallet, vilka effekter en kombination av de två ämnena ger. Vuxna zebrafiskar uppvisade beteendeförändringar även vid dessa låga koncentrationer efter två veckors exponering och de två ämnena påverkade beteendet olika var för sig och i kombination. Vidare, användes vildfångad storspigg i ett exponeringsexperiment för att undersöka om resultaten från zebrafisken, som är en avlad laboratoriefisk, kan ses också i vilda fiskpopulationer. Även storspiggar som exponerades för EE2 under utveckling fick ett modifierat beteende samt en skev könsfördelning som vuxna: fler honor fanns hos de storspiggar som exponerats och vidare undersökningar visade att dessa var genetiska hanar som utvecklats som honor.

Den här avhandlingen visar beständiga förändringar i zebrafiskens transkriptom i hjärna och testikelvävnad efter exponering för EE2 i låga halter under utveckling. Både icke-reproduktiva beteenden och fertilitet visade sig känsliga för EE2 i såväl zebrafisk som storspigg och effekterna verkar vara permanenta. Sammanfattningsvis har EE2 effekter på ekologiskt relevanta faktorer hos fisk i de halter som förekommer i vattenmiljön och hormonstörande föroreningar som EE2 kan ge långvariga effekter som syns senare i livet även vid låga koncentrationer.

sted, utgiver, år, opplag, sider
Huddinge: Södertörns högskola, 2018. s. 165
Serie
Södertörn Doctoral Dissertations, ISSN 1652-7399 ; 155
Emneord
17α-ethinylestradiol, endocrine disrupting chemical, fish, behavior, fertility, transcriptome, RNA sequencing
HSV kategori
Forskningsprogram
Miljövetenskapliga studier; Östersjö- och Östeuropaforskning
Identifikatorer
urn:nbn:se:sh:diva-34913 (URN)978-91-88663-43-6 (ISBN)978-91-88663-44-3 (ISBN)
Disputas
2018-06-01, MA624, Alfred Nobels allé 7, Huddinge, 10:00 (engelsk)
Opponent
Veileder
Forskningsfinansiär
The Foundation for Baltic and East European Studies
Tilgjengelig fra: 2018-05-08 Laget: 2018-04-30 Sist oppdatert: 2018-05-08bibliografisk kontrollert

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