Glucocorticoids and phenotypic programming in birds

Lead Research Organisation: University of St Andrews
Department Name: Psychology

Abstract

When an animal's environment changes unpredictably, for example during periods of bad weather or food shortages, they suffer stress. During this time specific chemical messengers, called stress hormones, are released into the bloodstream following a series of complex interactions within a hormonal system called the hypothalamic-pituitary-adrenal axis. In the short-term these hormones can benefit the animal as they promote activities such as foraging that help it survive. If the stress continues for a period of hours or days, however, these hormones can have harmful effects. If a mother lives in a stressful environment she can pass an increased level of stress hormones to her developing offspring, and we know that if animals experience high levels of these hormones while they are growing this can have long-term effects on how they behave when they are adults. These changes in behaviour are linked to a prolonged release of stress hormones in a stressful situation, due to a disruption in regulatory systems. Some of these effects are harmful, and early stress has been linked to health problems such as hypertension or diabetes, so it is very important that we understand the physiological mechanism underlying this system. The central aim of my research is to investigate this by looking at the effects of stress hormones on animals throughout their life cycle, concentrating my attention at different biological levels, quantifying changes in gene expression, physiology, behaviour and reproductive success. One exciting aspect of this study is that I will be able to directly manipulate the stress hormone levels of individuals and track their development and behaviour throughout life. This is possible as I have chosen to work on birds; because when the mother lays her egg she transfers all the nutrients and hormones required for embryonic growth at one time, and we know that this includes stress hormones. I will mimic a stressful environment by injecting small known amounts of stress hormones into these eggs. Whilst the traditional view of developmental stress is one of harmful effects, there is an intriguing alternative perspective. Mothers could capitalise on the physiological changes that occur following exposure to stress hormones to 'engineer' their offspring in order to prepare them for the environment they will live in once they are born, maximising their chances of survival. The negative effects seen in many studies could then be a case of the environment after birth not matching the one experienced by the mother. This is a novel idea that was proposed to explain why stress hormones have such long-term effects on animals. However, very few experiments have investigated this, even though it could provide information on how stress hormones might cause later health problems. I will tackle this important topic by carrying out experiments that create post-natal environments that match or mis-match the pre-natal conditions an animal experiences. I will then follow birds as they grow and test how well they breed under favourable and unfavourable conditions. Finally I can also track the development of these birds' offspring. This will be important in helping us understand how persistent change can occur across generations without changing the genetic code, a phenomenon called epigenetic inheritance. My research will provide novel information on the importance of early life conditions in shaping helping an individual to cope with its environment. This has significant implications for human and animal health programmes and animal breeding projects. A greater understanding of epigenetic inheritance is important not just to the scientific community but may be relevant to those concerned about climate change. This is due to its potential influence on the survival of populations under uncertain environmental conditions, a circumstance that may be relevant to human and non-human animals in the years to come.

Technical Summary

The potential influence that physiological conditions experienced during early development may have on adult phenotypes has recently developed as an important research focus. Mothers experiencing stressful conditions during pregnancy or egg-laying can transfer stress hormones to their offspring, manipulating pre-natal developmental conditions. This project will investigate the long-term and transgenerational effects of pre-natal exposure to stress hormones, specifically corticosterone (CORT) via laboratory based experiments using an avian species the Japanese quail. In particular, this research will examine the role of pre-natal corticosterone exposure on embryonic development, the physiological and behavioural responses to a range of stressors in adulthood, as well as reproductive success and long-term effects on offspring quality. The objectives will be met by studying embryonic and post-natal responses following a standardised pre-natal manipulation, namely the intra-ovo injection of a known amount of exogenous glucocorticoids. Birds will then be studied using an interdisciplinary approach, combining behavioural assay with radioimmunoassay (RIA) hormone profiling, magnetic resonance imaging (MRI), reverse transcription polymerase chain reaction (RT-PCR) and in situ hybridisation (ISH) techniques to track individual changes in neural development, stress axis functionality, physiology, behaviour and breeding success. This study takes a multi-disciplinary approach, drawing on endocrinology, behavioural ecology and reproductive physiology. This research will therefore provide detailed information on how early life CORT exposure could program the physiology of a bird throughout its life and how these effects could be felt in future generations. Taking such a long term approach, tracking individuals throughout their life cycle and applying an integrated approach will enable me to determine the potential for transgenerational epigenetic change in populations.

Publications

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Lovell PG (2013) Egg-laying substrate selection for optimal camouflage by quail. in Current biology : CB

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Boogert NJ (2014) Developmental stress predicts social network position. in Biology letters

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Zimmer C (2015) Reduced resistance to oxidative stress during reproduction as a cost of early-life stress. in Comparative biochemistry and physiology. Part A, Molecular & integrative physiology

Related Projects

Project Reference Relationship Related To Start End Award Value
BB/E024459/1 01/10/2007 01/04/2011 £695,952
BB/E024459/2 Transfer BB/E024459/1 02/04/2011 15/04/2014 £257,503
 
Description Several papers have been produced as part of this work. I have shown that early life experiences can drive behavioural change - creating phenotypes that are programmed to thrive in a matched environment. These behavioural traits are mediated by changes to the physiological stress response and also to changes in the neuroendocrine pathways in the brain. Each of these changes is passed on to the next generation.

We have now discovered that there is significant transgenerational transmission of several; phenotypic traits following pre-natal stress, despite offspring post-natal environments. These include behavioural traits that we can trace back to endocrine mechanisms and also to neuroendocrine disruption at the cellular level. Publication in press. Also further work on adolescence as a very sensitive period for altering later behaviour - modulation of stress or even social conditions during this time can have both positive and negative effects on coping strategies.
Exploitation Route I have given insight into welfare protocols, showing that pre-natal conditions are more important in driving behaviours that allow coping with stress than post-natal ones in poultry species. This could be used in welfare protocols.
Sectors Agriculture, Food and Drink,Environment,Pharmaceuticals and Medical Biotechnology

 
Description BSN research grant
Amount £3,000 (GBP)
Organisation University of St Andrews 
Sector Academic/University
Country United Kingdom
Start 09/2018 
End 06/2019
 
Description CASE Studentship
Amount £78,000 (GBP)
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 09/2017 
End 09/2021
 
Description EASTBIO studentship
Amount £88,000 (GBP)
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 09/2015 
End 09/2019
 
Description East Bio DTP studentship - Developmental programming of biological rhythms
Amount £88,000 (GBP)
Organisation University of St Andrews 
Sector Academic/University
Country United Kingdom
Start 09/2017 
End 09/2021
 
Description ISSF Wellcome Trust initiative
Amount £19,000 (GBP)
Organisation University of St Andrews 
Sector Academic/University
Country United Kingdom
Start 02/2017 
End 01/2018
 
Description ISSF Wellcome Trust initiative - Eggcellent Roadshow
Amount £13,000 (GBP)
Organisation University of St Andrews 
Sector Academic/University
Country United Kingdom
Start 04/2018 
End 08/2018
 
Description Impact Fund/KE - PokeHormoneGo roadshow funding.
Amount £5,000 (GBP)
Organisation University of St Andrews 
Sector Academic/University
Country United Kingdom
Start 05/2017 
End 01/2018
 
Description Leverhulme Trust Grant
Amount £107,000 (GBP)
Organisation The Leverhulme Trust 
Sector Charity/Non Profit
Country United Kingdom
Start 01/2015 
End 12/2017
 
Description RSE sabbatical award
Amount £64,000 (GBP)
Organisation University of St Andrews 
Sector Academic/University
Country United Kingdom
Start 01/2020 
End 12/2020
 
Description Responsive mode
Amount £750,000 (GBP)
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 02/2018 
End 01/2021
 
Description Emerging contaminants collaboration 
Organisation University of Glasgow
Country United Kingdom 
Sector Academic/University 
PI Contribution New collaboration looking at role of early life exposure to environmental contamination - bought in as avian expert - new collaboration
Collaborator Contribution NERC grant submitted, also some analysis of fecal samples run for our work.
Impact None yet
Start Year 2017
 
Description European collaboration on Avian Endocrinology 
Organisation Max Planck Society
Department Max Planck Institute for Ornithology
Country Germany 
Sector Academic/University 
PI Contribution Organisation of symposium at ECBB 2018, Current preparation of Marie Curie International Training Network grant Jan 2019, participation on two international meetings to cement collaboration
Collaborator Contribution As above - also leading the ITN application.
Impact Symposium organised for August 2018
Start Year 2017
 
Description European collaboration on Avian Endocrinology 
Organisation University of Groningen
Country Netherlands 
Sector Academic/University 
PI Contribution Organisation of symposium at ECBB 2018, Current preparation of Marie Curie International Training Network grant Jan 2019, participation on two international meetings to cement collaboration
Collaborator Contribution As above - also leading the ITN application.
Impact Symposium organised for August 2018
Start Year 2017
 
Description European collaboration on Avian Endocrinology 
Organisation University of Lisbon
Country Portugal 
Sector Academic/University 
PI Contribution Organisation of symposium at ECBB 2018, Current preparation of Marie Curie International Training Network grant Jan 2019, participation on two international meetings to cement collaboration
Collaborator Contribution As above - also leading the ITN application.
Impact Symposium organised for August 2018
Start Year 2017
 
Description European collaboration on Avian Endocrinology 
Organisation University of Veterinary Medicine Vienna
Country Austria 
Sector Academic/University 
PI Contribution Organisation of symposium at ECBB 2018, Current preparation of Marie Curie International Training Network grant Jan 2019, participation on two international meetings to cement collaboration
Collaborator Contribution As above - also leading the ITN application.
Impact Symposium organised for August 2018
Start Year 2017
 
Description Field based endorcinology 
Organisation Pittarthie Farm
Country United Kingdom 
Sector Private 
PI Contribution Collaboration with local landowner to set up nest box populations for field based endocrinology - new collaboration
Collaborator Contribution Provision of research area and land use.
Impact None as yet
Start Year 2017
 
Description Seabird health and development 
Organisation British Trust for Ornithology
Country United Kingdom 
Sector Charity/Non Profit 
PI Contribution Assisting with monitoring health of tracked seabirds in the UK, adding valuable physiological assays. Linking use of anthropogenic environments (feeding sources) to alterations in seabird development post-natally and egg quality.
Collaborator Contribution Expertise in tracking and assistance with field locations.
Impact PhD studentship 2017- 2021, NERC Case Joint applications for funding (pending)
Start Year 2017
 
Description Development of PE pages in group website 
Form Of Engagement Activity Engagement focused website, blog or social media channel
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact We have developed a new website showcasing our research and alongside this we have created PE activity pages, with a dedicated form for PE involvement by several sectors, including schools. We have not assessed hot rates yet and whilst the pages were developed in 2018, the site was only launched in Feb 2019. WE will endeavour to monitor the impacts via correspondence we receive to engage with schools etc. Already 5 schools have contacted us about our Schools roadshow.
Year(s) Of Engagement Activity 2018
URL https://www.moblabgroup.com/public-engagement-outreach
 
Description Development of interactive app - several national science festivals attended 
Form Of Engagement Activity Engagement focused website, blog or social media channel
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact 4 major festivals attended - development of interactive app for explanation of research
Year(s) Of Engagement Activity 2017,2018
 
Description Interaction with industry 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Industry/Business
Results and Impact Invited participation to act on an advisory team consisting of representatives at Stonegate Ltd, Clarence Court Eggs Ltd, Crediton Milling (feed supplier), Premier Nutrition and a range of small scale egg producers who work with the company. My work with this group has already resulted in changes to housing conditions and we are now undertaking joint research projects in order to maximise welfare and egg production in socially housed birds.
Year(s) Of Engagement Activity 2019
 
Description Organisation of Science Fair St Andrews 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Science fair organisation - annual event organised by myself.
Year(s) Of Engagement Activity 2016,2017
 
Description Outreach at primary schools 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact PI is currently running an Easter themed activity with local Primary schools. Information given is based on the research being undertaken. Children are incubating and hatching out their own chick sin tie for Easter. Levels involved include P1-P7. media coverage expected in mid March 2016 and further projects like this planned for next year on a larger scale
Year(s) Of Engagement Activity 2016
 
Description Participation in Science fair (UK wide) 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Attendance at National science fair with Hypothalamus Hunt app, related to research undertaken on grant. Over 500 members of the general public attended and feedback was highly favourable. App has continued to gather downloads from IOS and Android platforms.
Year(s) Of Engagement Activity 2018
URL https://pocketsizedhands.com/our-work/HypothalamusHunt/
 
Description Participation in explorathon 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Exploration night at Byre Theatre. Stall involving several aspects of group research.
Year(s) Of Engagement Activity 2016
URL http://www.explorathon.co.uk/
 
Description Schools roadshow 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Schools
Results and Impact Roadshow based on the App we developed.
Year(s) Of Engagement Activity 2017,2018
 
Description Schools roadshow - developmental biology 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Schools
Results and Impact Schools roadshow developed to increase understanding of general developmental biology principles. Interactive sessions (3-4 per class over 4 weeks) at Primary and Pre-school institutions all over Fife and Angus, including special needs units in Dundee. In total 17 institutions were visited reaching multiple classes within these schools. Our work engaged 854 pupils, with 50% of these at pre-school levels. In each of these nurseries we reached the entire cohort. Primary school sessions ranged from P1-6. We have had requests for a more widespread program this year (2019), however funding will be required. In 2019 we have scaled this to 6 institutions due to funding issues.
Year(s) Of Engagement Activity 2018
URL https://www.moblabgroup.com/public-engagement-outreach