Neurological adaptation and ecological specialisation

Lead Research Organisation: University of Bristol
Department Name: Biological Sciences

Abstract

We live amidst a cacophony of sensory information. It is the job of the brain to make sense of the environment we live in. It must extract the most relevant cues and combine this information with memories of past experiences to trigger appropriate behavioural responses. For animals living in different environments the most reliable sensory information may come from different sources, the experiences they have may vary, and what passes as appropriate behaviour can be radically different. The brain must therefore evolve to meet the demands of a changing environment. My research asks how brains accommodate adaptive change, how these changes are brought about, and why one evolutionary solution is favoured over another.

For over 150 years biologists have studied mimetic butterflies to gain insights into the evolutionary process. Mimicry evolves when distantly related species converge on the same colour pattern to warn predators that they are toxic and to be avoided. This has dramatic knock-on effects, driving changes in habitat preference, sensory environment, foraging and reproductive behaviour. In many cases it results in butterflies that evolved to look the same also behaving in similar ways and occupying similar habitats. This makes them an ideal system to study how brains function and evolve because they are behaviourally diverse and the same behaviours have evolved multiple times.

My project leverages these features to explore how brain structure changes as species diverge into different environments. I will measure the size of distinct components of the brain that have different functions, for example in vision, olfaction or memory. Changes in their relative size imply a change in the importance of that function. By comparing brains of different species I can therefore identify differences in their structure that reflect adaptations to the particular demands of a species' environment. I will then ask how these changes occur: are they are the result of genetic changes or flexibility in the way the brain develops? And how do changes at the cellular level alter the way the brain processes and stores information?

Understanding how brains evolve is central to understanding the diverse range of behaviour observed in the animal kingdom, a major axis of biodiversity. It can also tell us how quickly animals are able to change their behaviour to respond to rapid environmental change, and whether this requires selection for genetically-encoded adaptations, or if it can be facilitated by flexibility in the way brains and behaviour develop.

Evolutionary comparisons also provide insightful models for general problems in understanding brain function. For example, what types of cells contribute to changes in brain size? How is brain development controlled? And how do different brain cells connect and communicate with one another? This can tell us about our own biology, and the origin of disorders caused by disruption of these developmental processes.

I will tackle these questions by homing in on specific changes in the way species perceive and remember information about their environment. For example, I have previously shown that one brain region, called the mushroom body, has trebled in size in passion-vine butterflies. The mushroom bodies are implicated in learning and memory, and this explosive expansion may be linked to the skill with which these species navigate their environment. Similarities in the genetic control and functional organisation of the insect mushroom body make it directly comparable to the mammalian forebrain, providing a novel framework for studying general principles in cell proliferation and communication. By considering how mushroom body expansion occurred at multiple biological levels, from genes to cells to behaviour and ecology, I will investigate how processes at these different scales interact to facilitate, or restrict, the way brains function.

Planned Impact

A) Who will benefit from this research?

1. Teachers and students of ecology and evolution, and neuroscience
2. The public
3. Owners/managers of butterfly houses and museum exhibits
4. Conservation and environmental agencies

B) How will they benefit from this research?

1. I will work with local schools, some of which are currently under OFSTED 'special measures', and create an online resource to convey key concepts in ecology, evolution and neuroscience in an accessible format to promote enthusiasm and interest in STEM subjects. Collaboration between schools and local scientists can significantly enhance a school student's enthusiasm for science. For example, in a recent STEMNET report over 80% of teachers reported an increase in pupil engagement, and over 70% reported an increase in understanding of STEM subjects after contact with local scientists. The project is well suited for this purpose as it addresses multiple broad concepts covered in GCSE and A-level biology syllabuses:
i) Ecology and evolution: The project exemplifies core topics in GCSE and A-level syllabus such as the role ecology plays in shaping biodiversity, interactions between individuals and their environment, co-evolution between flowering plants and foraging insects, the process of adaptation, and the role plasticity plays in diversification. The accessibility and popularity of the study species, and the enigmatic nature of the Neotropics aid communication of these important concepts.
ii) Neuroscience: This project tackles key concepts in neuroscience in an accessible system where the wider ecological importance can be clearly conveyed. This provides a means to introduce core subjects in school syllabuses such as how organisms respond to changes in their internal and external environments, and how receptors and nerve cells function.
I will engage with local schools through the STEMNET ambassador scheme, the Nuffield Foundation research placement scheme, and by renewing previous links schools.

2. There is huge enthusiasm for science among the UK public. The 2014 State of Public Attitudes to Science Ipsos-Mori poll found an overwhelming majority (72%) of the public believe it is important to know about science for the daily life, but a majority (58%) also felt scientists put too little effort into informing the public amount their work. Tropical rainforests, brightly coloured butterflies, and weird looking brains offer an enticing combination for a general audience. I will be proactive about using these features to communicate my work, and the importance of the broader concepts, to the wider public through press-releases, community engagement schemes, scientific writing and exploiting existing podcasts based in Cambridge, and my prior experience with multimedia companies. The popularity of the Cambridge Science Festival, Festival of Ideas and the active outreach programs of the University Museums provide ideal opportunities to convey to the importance and excitement of my research to the public.

3. Brightly coloured butterflies are common species in tropical butterfly houses and exhibits, offering an opportunity to communicate scientific concepts in conjunction with popular displays of biodiversity. I will be proactive about establishing connections with butterfly houses in South East England (eg Tropical Wings Zoo, Chelmsford, Shepreth Wildlife Park, and Colchester Zoo), as well as local Zoology museums to collaborate on developing educational resources.

4. Understanding how populations can adapt to rapid environmental change is crucial to understanding the likely effects of climate change on biodiversity. This project will contribute to this understanding by assessing rates of change in brain structure during ecological divergence. By quantifying the relative contribution of plasticity to this process I will address whether plasticity is likely to provide a means by which species can negotiate rapid changes in their environment.

Publications

10 25 50

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Barton RA (2019) Proportional versus relative size as metrics in human brain evolution. in Proceedings of the National Academy of Sciences of the United States of America

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King SL (2022) Social and vocal complexity in bottlenose dolphins. in Trends in neurosciences

 
Description I have developed a second substantial research program in Neotropical butterflies that aims integrate ecological and phylogenetic data, comparative genomics and development, and neuroanatomy to tackle major questions in evolutionary neurobiology. This work has documented a series of striking neural adaptations, including one of the most explosive shifts in neuroanatomy documented to date, and a peculiar case of an olfactory adaptation lost at the origin of butterflies, re-evolving in the Ithomiini. I have also shown that local adaptation across environmental gradients leads to broad changes in both neuroanatomy and neural gene expression, particularly affecting sensory pathways, strongly suggesting the brain plays a hitherto unappreciated role in facilitating speciation.
Exploitation Route We have established new model systems for investigating behavioural evolution, and are establishing tools to advance our exploratory power in these contexts. These systems, tools and the data we generate will be of broader benefit to the academic community. Our work has also resulted in several outreach projects which contribute to the cultural and educational basis of the publics connection with the environment, and scientific research.
Sectors Education,Environment,Culture, Heritage, Museums and Collections,Other

 
Description ERC Starter Grant
Amount € 1,499,940 (EUR)
Funding ID 758508 
Organisation European Research Council (ERC) 
Sector Public
Country Belgium
Start 02/2018 
End 02/2023
 
Description NERC GW4+ DTP Studentship to Benito Wainwright
Amount £92,000 (GBP)
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 09/2019 
End 02/2023
 
Description SWBio BBSRC DTP Studentship to Amaia Alcalde
Amount £92,000 (GBP)
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 10/2022 
End 09/2026
 
Description SWBio BBSRC DTP Studentship to Callum McClellan
Amount £92,000 (GBP)
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 09/2019 
End 08/2023
 
Description SWBio MRC DTP Studentship to Jessica Foley
Amount £92,000 (GBP)
Organisation Medical Research Council (MRC) 
Sector Public
Country United Kingdom
Start 10/2020 
End 09/2024
 
Description The neural basis of kin recognition in social insects
Amount £271,376 (GBP)
Funding ID RPG-2019-287 
Organisation The Leverhulme Trust 
Sector Charity/Non Profit
Country United Kingdom
Start 06/2020 
End 05/2023
 
Description Brains and Speciation: Collaborations with Dr Richard Merrill 
Organisation Ludwig Maximilian University of Munich (LMU Munich)
Country Germany 
Sector Academic/University 
PI Contribution We are collaborators on an ERC Grant investigating neural and behavioural divergence during the early stages of speciation. We are collaborating on studies investigating divergence in brain anatomy and how these relate to behavioural differences.
Collaborator Contribution Our collaborator, Dr Richard Merrill, is the Principal Investigator on the grant and leads and coordinates the project.
Impact The project is at an early stage.
Start Year 2020
 
Description EVOKIN: collaborating with Jean Christophe Sandoz on an ANR project 
Organisation University Paris Sud
Country France 
Sector Academic/University 
PI Contribution We co-authored a proposal to the ANR (the French National funding agency) to complaint our recent Leverhulme Trust grant with more physiological and behavioural techniques. We co-authored the proposal and will be co-investigators on the project.
Collaborator Contribution Our collaborator, Dr Jean Christophe Sandoz, lead the proposal application and is lead investigator on the project.
Impact The project is at an early stage.
Start Year 2021
 
Description Foraging ecology of Heliconius butterflies 
Organisation Federal University of Rio de Janeiro
Country Brazil 
Sector Academic/University 
PI Contribution I am collaborating with Prof Márcio Cardoso, with whom I co-supervise a PhD student, Priscila Moura, on a project on the evolutionary ecology of Heliconius foraging behaviour.
Collaborator Contribution Intellectional and organisational collaboration.
Impact Moura PA, Corso G, Montgomery SH, Cardoso MZ. True site fidelity in Heliconius butterflies. Fun. Ecol. in press.
Start Year 2018
 
Description Lepidopteran neurobiology 
Organisation George Washington University
Country United States 
Sector Academic/University 
PI Contribution Jointly lead a research grant from the HFSP
Collaborator Contribution Jointly lead a research grant from the HFSP
Impact The collaboration is multi-disciplinary, combining evolutionary biology, neuroscience, physiology and molecular biology.
Start Year 2022
 
Description Lepidopteran neurobiology 
Organisation Norwegian University of Science and Technology (NTNU)
Country Norway 
Sector Academic/University 
PI Contribution Jointly lead a research grant from the HFSP
Collaborator Contribution Jointly lead a research grant from the HFSP
Impact The collaboration is multi-disciplinary, combining evolutionary biology, neuroscience, physiology and molecular biology.
Start Year 2022
 
Description Lepidopteran neurobiology 
Organisation Universidad Regional Amazónica IKIAM
Country Ecuador 
Sector Academic/University 
PI Contribution Jointly lead a research grant from the HFSP
Collaborator Contribution Jointly lead a research grant from the HFSP
Impact The collaboration is multi-disciplinary, combining evolutionary biology, neuroscience, physiology and molecular biology.
Start Year 2022
 
Description Black History Month exhibition 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Undergraduate students
Results and Impact Exhibition on influential black biologists throughout history.
Year(s) Of Engagement Activity 2022
 
Description Charles Henry Turner display 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Undergraduate students
Results and Impact I created a display about Charles Henry Turner, a black biologist of historical significance, who's impact has been marginalised. The exhibit is for permanent display in the Life Science Building, University of Bristol, and aims to increase awareness of black figures in the subject, primarily aimed at our black undergraduate students.
Year(s) Of Engagement Activity 2022
 
Description Connections: Science and Poetry 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact This was a collaboration between six scientists and six poets to try and capture the nature and subject of research in a new way, run by Murray Edwards College Cambridge. The project spanned the pandemic and included a second session on the impact of Covid on Universities.
Year(s) Of Engagement Activity 2019,2020
 
Description Mariposters: educational material on butterfly biology 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact We created 14 posters about butterfly biology with the Smithsonian Tropical Research Institute. These were translated into 9 languages and are freely available to be downloaded. The website is still being finalised but material is already being accessed and used.
Year(s) Of Engagement Activity 2020,2021
URL https://striresearch.si.edu/mariposters/