Integrative analysis of serotonin-mediated behavioural phase transition in the desert locust
Lead Research Organisation:
University of Leicester
Department Name: Biology
Abstract
Animals may undergo profound changes in their behaviour, body shape and colour in response to varying environmental conditions. This poses a major problem in biology: how do the surroundings in which an animal lives, influence the expression of its genes and mould its brain function, its hormones, and hence its behaviour, so that it is appropriately adapted to changing circumstances. The Desert Locust shows an extreme example of this malleability; it can change reversibly from a shy and inconspicuous, solitary creature that flies at night to one that is highly conspicuous, day flying and occasionally aggregates in vast numbers which has devastating economic effects. These two forms - the solitarious and gregarious phases - are strikingly different in appearance, physiology and behaviour. They can be bred in the laboratory and made to switch from one phase to the other and back, by simply raising them in isolation or in a crowd. They have relatively few nerve cells in their brain so that it is possible to understand the changes that occur during these phase transitions and to illuminate the similar mechanisms that occur in more complex animals when they find themselves in new circumstances. The key decision a locust must make is to join with or avoid other locusts. Once this has been made subsequent changes in physiology, body shape and colour follow from the continuing presence or absence of other locusts. Tickling the hind legs of a solitarious locust to mimic the effects of jostling with others, or the sight and smell of other locusts, can, in 1-2 h, cause the behaviour to become gregarious. This transition is accompanied by substantial changes in the amounts of many chemicals in its nervous system. In particular serotonin (a substance that in human brains affects many moods such as aggression and depression, and the release of which is affected by drugs such as ecstasy) shows a large but short-lived increase and, critically, it is both necessary and sufficient to induce the change in behaviour. We have determined which nerve cells show changes in their serotonin levels. We now wish to understand how serotonin changes the workings of nerve cells to bring about the transformation of behaviour. To achieve this aim we have these key objectives: 1. Identify and characterise the nerve cells that change their production of serotonin during the initial change in behaviour. How far do they extend through the central nervous system? How do they respond in the presence of other locusts, and what effects do they have on other nerve cells to bring about changes in behaviour? 2. Identify the nerve cells that are influenced by the release of serotonin. What chemical changes does serotonin cause in the internal workings of these nerve cells? This will be examined at the level of specific molecules that engage in cascades of chemical reactions to pass information within one cell and to neighbours. 3. Serotonin can change the effectiveness and the time course of communication between nerve cells, providing an essential building block of learning. How do differing amounts of serotonin in the nervous system before, during and after the experience of crowding, affect communication between nerve cells? Does serotonin have different effects in solitarious and gregarious locusts? 4. Examine in detail how solitarious and gregarious locusts differ in their patterns of daily activity such as feeding, exploring their environment and sleeping, and begin to look at how genes that regulate their body clock differ in the two phases. 5. Gregarious locusts quickly revert to solitarious behaviour if they are removed from the crowd. What are the mechanisms that maintain their gregarious behaviour and what is the complimentary process that leads to solitarious behaviour?
Technical Summary
How does the interplay between the environment and gene expression mould brain function and behaviour so that an animal can adapt to changing circumstances? Desert Locusts show an extreme form of this phenotypic plasticity by changing from a shy animal, cryptic in appearance and avoiding other locusts, to one that lives in large groups, has bright warning colours as nymphs and is actively attracted to other locusts. We wish to capitalise on our recent breakthrough in identifying serotonin (5HT) as underlying the transformation from solitarious to gregarious behaviour, and our identification of neurons that up-regulate 5HT within 1 h of receiving gregarizing stimuli. We wish to build on these data by using a systems approach to identifying the sequence of processes, at molecular, cellular and neural levels that link the increased release of 5HT with changes of neuronal function and behaviour in this tractable model. We have these key objectives: 1. Characterise the anatomy and physiology of the individual serotonergic neurons that up-regulate 5HT production during behavioural gregarization. 2. Identify the targets of 5HT-mediated plasticity during phase change. We will determine: the targets of PKA phosphorylation both i) at the cellular level by identifying the anatomical location of neurons affected by gregarization and ii) at the molecular level, within neurons. 3. Determine how altered physiological function underlies the changes associated with behavioural gregarization. We will analyse how serotonin affects the physiology of identified neurons, before, during and after phase change. 4. Determine the behavioural consequences of phase change on circadian rhythms and aggregation. 5. Determine how the gregarious phase is maintained and how it is lost during the process of behavioural solitarization that occurs when gregarious locusts are isolated from the crowd.
Publications
Badisco L
(2011)
Microarray-based transcriptomic analysis of differences between long-term gregarious and solitarious desert locusts.
in PloS one
Blackburn LM
(2010)
Motor neurone responses during a postural reflex in solitarious and gregarious desert locusts.
in Journal of insect physiology
Matheson T
(2012)
The Insects - Structure and Function
Nielsen TA
(2012)
A formal mathematical framework for physiological observations, experiments and analyses.
in Journal of the Royal Society, Interface
Nielsen TA, Matheson T, Nilsson H
(2010)
Trends in Functional Programming
Rogers SM
(2014)
Rapid behavioural gregarization in the desert locust, Schistocerca gregaria entails synchronous changes in both activity and attraction to conspecifics.
in Journal of insect physiology
Description | The Desert Locust can change reversibly from a shy and inconspicuous, solitary creature that flies at night to one that is highly conspicuous, day flying and occasionally aggregates in vast numbers which has devastating economic effects. These two forms - the solitarious and gregarious phases - are strikingly different in appearance, physiology and behaviour. Our research seeks to understand changes in the nervous system that accompany this transformation. We have made a major contribution to the understanding of mechanisms underlying locust phase change (swarming) Rogers et al. 2014 Journal of Insect Physiology 65: 9-26). We have developed a broad mathematical framework for the analysis of physiological data (Nielsen et al. 2012 J. Roy Soc. Interface 9: 1040-1050). This work has both conceptual and practical importance, and we have formed a spinout company Openbrain Ltd to commercialise aspects of this.. We have described differences in the walking posture and motor control of limb movements in solitarious and gregarious locusts (Rogers et al. 2010. J. Ins. Physiol. 56: 902-910. The differences can be related to the cryptic (camouflaged) behaviour of solitarious locusts. We have demonstrated (Badisco et al. 2011. PLoS One 6: e28110) that patterns of gene expression differ markedly in solitarious and gregarious locusts. This work highlights specific physiological differences between the two phases, and provides key data for further analyses of locust phase change. We have participated in national and international collaborations, presented our results at universities and international conferences, trained students and obtained follow on funding to develop some aspects of our work. |
Exploitation Route | Our data analysis tool developed for the analysis of electrophysiological recordings uses statistical models that are shared with (for example) financial applications and clinical diagnostics. We are exploring potential applications in such non-academic contexts. To meet the data analysis needs of the work in this grant application, we have developed a generally applicable software tool for statistical modelling and Bayesian inference. With assistance from the University of Leicester Enterprise and Business Development Unit, we are seeking to commercialise this tool. |
Sectors | Digital/Communication/Information Technologies (including Software),Education,Energy,Financial Services, and Management Consultancy,Healthcare,Retail |
URL | http://www2.le.ac.uk/departments/biology/people/matheson/research/current/phase |
Description | I am not able to formally assess how our research into the mechanisms underyling swarming behaviour in locusts may have influenced locust control to date. In the long term I expect that through it's contribution to our understanind of locust biology it will have such impacts, but these may be very difficult to track back to this or any other specific grant. I have provided expert advice to the media regarding the 2020 locust swarm crisis threatening East Africa. |
Description | Development of advanced level in vivo electrophysiology training material |
Geographic Reach | Local/Municipal/Regional |
Policy Influence Type | Influenced training of practitioners or researchers |
Impact | Course provides advanced training in electrophysiological techniques underpinning in vivo research to 6 PhD level researchers per year. Open to BBSRC and Institutionally funded researchers from the Midlands region, UK. |
Description | NC3Rs Expert Working Group on Impact |
Geographic Reach | National |
Policy Influence Type | Membership of a guideline committee |
Impact | National level funding body guidance on impact generation in the area of improved animal welfare. |
Description | 14ALERT |
Amount | £638,019 (GBP) |
Funding ID | BB/M012034/1 |
Organisation | Biotechnology and Biological Sciences Research Council (BBSRC) |
Sector | Public |
Country | United Kingdom |
Start | 01/2015 |
End | 01/2016 |
Description | BBSRC Responsive Mode Research Grants |
Amount | £689,981 (GBP) |
Funding ID | BB/L02389X/1 |
Organisation | Biotechnology and Biological Sciences Research Council (BBSRC) |
Sector | Public |
Country | United Kingdom |
Start | 11/2014 |
End | 01/2018 |
Description | Circadian plasticity in the visual system |
Amount | £74,800 (GBP) |
Funding ID | BB/F016727/1 |
Organisation | Biotechnology and Biological Sciences Research Council (BBSRC) |
Sector | Public |
Country | United Kingdom |
Start | 10/2011 |
End | 09/2015 |
Description | Insect Allergens in Future Foods and Workplaces |
Amount | £10,000 (GBP) |
Funding ID | KEEF2019 |
Organisation | University of Leicester |
Sector | Academic/University |
Country | United Kingdom |
Start | 08/2019 |
End | 07/2020 |
Title | Automated video analysis of behaviour of adult locusts. |
Description | A novel analysis technique for assessing rhythmic behaviour in adult locusts using digital video recording and automated video analysis software (EthoVision). |
Type Of Material | Technology assay or reagent |
Provided To Others? | No |
Impact | None to date. |
Title | Behavioural assay for phase-state determination in adult locusts. |
Description | A behavioural assay, based on data obtained from automated video analysis of adult locusts, has been developed and used to produce a gregarization index by means of binary logistic regression. |
Type Of Material | Technology assay or reagent |
Provided To Others? | No |
Impact | None to date. |
Title | Development of solitarious locust facility and techniques to rear and work with solitarious and gregarious locusts |
Description | Development of world-leading state-of-the-art solitarious (isolated) locust facility and techniques to rear and work with solitarious and gregarious locusts. Space to quarantine field-sourced animals and carry out experimental protocols. Crucial to support research into mechanisms of locust swarming. |
Type Of Material | Improvements to research infrastructure |
Year Produced | 2015 |
Provided To Others? | Yes |
Impact | New collaborations (Ould Babah, Mauritania; Fonseca, Brazil). TV documentary (Back2back Productions). Showpiece at University Open Days influencing career decisions of many undergraduate students. |
Title | uHPLC analysis of biogenic amines |
Description | Development of protocols to assay biogenic amines in insect tissues |
Type Of Material | Physiological assessment or outcome measure |
Year Produced | 2017 |
Provided To Others? | Yes |
Impact | Development of new research collaborations |
Description | Collaboration with Duane Fonseca |
Organisation | Federal University of Minas Gerais |
Department | Institute of Biological Sciences |
Country | Brazil |
Sector | Academic/University |
PI Contribution | Hosted visiting international researcher on several occasions, provided experimental material, equipment and expertise. |
Collaborator Contribution | Fully funded the research visits by Brazilian researcher. |
Impact | In progress. |
Start Year | 2012 |
Description | Openbrain |
Organisation | OpenBrain |
Country | United Kingdom |
Sector | Private |
PI Contribution | Joint research into commercial development of research analytics. |
Collaborator Contribution | Joint research into commercial development of research analytics. |
Impact | BBSRC Follow on Fund Grant supports the partnership. Biology / mathematics / statistics. |
Start Year | 2012 |
Description | Research and Collaboration Agreement with the Universities of Cambridge and Leuven (Cambridge part) |
Organisation | University of Cambridge |
Country | United Kingdom |
Sector | Academic/University |
PI Contribution | The University of Cambridge, University of Leicester, and the Catholic University of Leuven, Belgium, have entered a formal Research and Collaboration Agreement for joint work on "Molecular Aspects of Locust Development". The specific objective of the Agreement is for the partners to "develop a technology to (i) identify transcripts responsible for polyphenism in locusts and (ii) investigate how patterns of gene expression relate to the animals behaviour, physiology and morphology." |
Start Year | 2008 |
Description | Research and Collaboration agreement with the Universities of Cambridge and Leuven (Leuven part) |
Organisation | Catholic University of Louvain |
Country | Belgium |
Sector | Academic/University |
PI Contribution | The University of Cambridge, University of Leicester, and the Catholic University of Leuven, Belgium, have entered a formal Research and Collaboration Agreement for joint work on "Molecular Aspects of Locust Development". The specific objective of the Agreement is for the partners to "develop a technology to (i) identify transcripts responsible for polyphenism in locusts and (ii) investigate how patterns of gene expression relate to the animals behaviour, physiology and morphology." |
Start Year | 2008 |
Title | Automated video analysis of behaviour of adult locusts. |
Description | A novel analysis technique for assessing rhythmic behaviour in adult locusts using digital video recording and automated video analysis software (EthoVision). |
Type Of Technology | New/Improved Technique/Technology |
Year Produced | 2011 |
Impact | None to date. |
Title | Calculus of Physiological Evidence |
Description | We have implemented a programming language for executing and analysing physiological experiments. |
Type Of Technology | Software |
Year Produced | 2011 |
Impact | Led to development of Spinout Company Openbrain Ltd. |
URL | http://www.cs.nott.ac.uk/~nhn/Publications/INCFUK2009Poster.pdf |
Company Name | Openbrain Ltd |
Description | Analytics development. |
Year Established | 2012 |
Impact | Commercially sensitive information. |
Website | http://openbrain.co.uk/ |
Description | Back2Back TV production |
Form Of Engagement Activity | A broadcast e.g. TV/radio/film/podcast (other than news/press) |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Public/other audiences |
Results and Impact | Tom Matheson and Swidbert Ott provided experimental material and expertise to an independent television production company, Back2Back Productions, in the course of making the broadcast TV programme 'Richard E Grant's Seven Deadly Sins: Gluttony', shown on Sky TV, Discovery Channel and available Online. |
Year(s) Of Engagement Activity | 2015 |
URL | http://www.back2back.tv/programmes/programdetail/?pt=srs&pid=1000112 |
Description | Bayesian analysis of physiological evidence. |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | local |
Primary Audience | Postgraduate students |
Results and Impact | Thomas Nielsen presented the results of our research in a seminar given to the Department of Biology, University of Leicester. no actual impacts realised to date |
Year(s) Of Engagement Activity | 2010 |
Description | Brain Awareness Day Events |
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 | Tom Matheson and members of the research group carried out live hands-on demonstrations of insect electrophysiology, exhibited live locusts, and displayed posters related to our research. |
Year(s) Of Engagement Activity | 2014,2016,2017 |
Description | Mathematically founded languages for experimental science: A mere curiosity, or should you really care? |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | international |
Primary Audience | Participants in your research or patient groups |
Results and Impact | Henrik Nilsson presented the results of our research in a talk given to the Computer Science department at University of Nottingham, Malaysia Campus. no actual impacts realised to date |
Year(s) Of Engagement Activity | 2011 |
Description | Vision, circadian rhythms and limb motor control in locusts |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | National |
Primary Audience | Postgraduate students |
Results and Impact | TM gave an Invited research talk at the University of Aberdeen Medical School. no actual impacts realised to date |
Year(s) Of Engagement Activity | 2012 |