Neurological adaptation and ecological specialisation

Lead Research Organisation: University of Cambridge
Department Name: Zoology

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
 
Description Balfour-Browne Trust Fund
Amount £935 (GBP)
Funding ID Award to support student project by Yiqing Wang 
Organisation University of Cambridge 
Sector Academic/University
Country United Kingdom
Start 08/2017 
End 06/2018
 
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 The Isaac Newton Trust/Wellcome Trust ISSF/University of Cambridge Joint Research Grants Scheme
Amount £49,745 (GBP)
Organisation University of Cambridge 
Department Isaac Newton Trust
Sector Academic/University
Country United Kingdom
Start 07/2017 
End 07/2018
 
Description Trinity College Graduate Studentship
Amount £126,105 (GBP)
Funding ID PhD studentship for Fletcher Young 
Organisation University of Cambridge 
Department Trinity College Cambridge
Sector Academic/University
Country United Kingdom
Start 10/2017 
End 09/2020
 
Title Data for: Neural divergence and hybrid disruption between ecologically isolated Heliconius butterflies 
Description The importance of behavioral evolution during speciation is well established, but we know little about how this is manifest in sensory and neural systems. A handful of studies have linked specific neural changes to divergence in host or mate preferences associated with speciation. However, the degree to which brains are adapted to local environmental conditions, and whether this contributes to reproductive isolation between close relatives that have diverged in ecology, remains unknown. Here, we examine divergence in brain morphology and neural gene expression between closely related, but ecologically distinct, Heliconius butterflies. Despite on-going gene flow, sympatric species pairs within the melpomene-cydno complex are consistently separated across a gradient of open to closed forest and decreasing light intensity. By generating quantitative neuroanatomical data for 107 butterflies, we show that H. melpomene and H. cydno clades have substantial shifts in brain morphology across their geographic range, with divergent structures clustered in the visual system. These neuroanatomical differences are mirrored by extensive divergence in neural gene expression. Differences in both neural morphology and gene expression are heritable, exceed expected rates of neutral divergence, and result in intermediate traits in first generation hybrid offspring. Strong evidence of divergent selection implies local adaptation to distinct selective optima in each parental microhabitat, suggesting the intermediate traits of hybrids are poorly matched to either condition. Neural traits may therefore contribute to coincident barriers to gene flow, thereby helping to facilitate speciation. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.7wm37pvs3
 
Title Divergence in Heliconius flight behaviour is associated with local adaptation to different forest structures 
Description Micro-habitat choice plays a major role in shaping local patterns of biodiversity. In butterflies, stratification in flight height has an important role in maintaining community diversity. The speciation in Heliconius butterflies is often associated with strong assortative mating, but ecological isolation and local adaptation is also considered essential. Despite its presumed importance, the role of behavioural shifts in early stages of speciation in response to differences in habitat structure is yet to be established. Here, we investigated variation in flight height behaviour in two closely related species, H. erato cyrbia and H. himera, which produce viable hybrids but are isolated across an environmental gradient, spanning lowland wet forest to high altitude scrub forest. We show that the two species fly at different heights in the wild, and demonstrate that this can be explained by differences in the vertical distribution of plant resources. We subsequently explored whether this divergence in flight height has a genetic component using common garden experiments. In both the wild and captivity, H. himera choose to fly lower and feed at lower positions, mirroring differences in resource availability in the wild. We suggest that this shift in foraging behaviour may reflect local adaptation to divergent forest structures highlighting the role of behaviour during early stages of speciation. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.msbcc2fx8
 
Title Re-emergence and diversification of a specialised antennal lobe morphology in ithomiine butterflies 
Description How an organism's sensory system functions is central to how it navigates its environment. The insect olfactory system is a prominent model for investigating how ecological factors impact sensory reception and processing. Notably, work in Lepidoptera led to the discovery of vastly expanded structures, termed macroglomerular complexes (MGCs), within the primary olfactory processing centre. MGCs typically process pheromonal cues, are usually larger in males, and provide classic examples of how variation in the size of neural structures reflects the importance of sensory cues. Though prevalent across moths, MGCs were lost during the origin of butterflies, consistent with evidence that courtship initiation in butterflies is primarily reliant on visual cues, rather than long distance chemical signals. However, an MGC was recently described in a species of ithomiine butterfly, suggesting that this once lost neural adaptation has re-emerged in this tribe. Here, we show that MGC-like morphologies are widely distributed across ithomiines, but vary in both their structure and prevalence of sexual dimorphism. Based on this interspecific variation we suggest that the ithomiine MGC is involved in processing both plant and pheromonal cues, which have similarities in their chemical constitution, and co-evolved with an increased importance of plant derived chemical compounds. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.8sf7m0cp5
 
Title Research data supporting 'Pollen-feeding delays reproductive senescence and maintains toxicity of Heliconius butterflies' 
Description The dataset has information about Heliconius erato demophoon butterflies fed for 14d (young) and 45d (old) on three different diets: sugar only (N); sugar + supplement (C) ; sugar + pollen from flowers (F). These experiments were set up with 8 males and 8 females of similar size (~3 cm of forewing radius) per treatment (diet/age). At the end of the experiment, females were individually assay for fertility: number of laid eggs recorded and the total eggs per females collected for quantification of cyanogenic glucosides (CG) using target-metabolomic (HPLC-MS/MS). Recently ecloded butterflies (0d, unfed) was also collected as a baseline. All butterflies were also weighted and collected for target metabolomics at the end of the experiment. 
Type Of Material Database/Collection of data 
Year Produced 2023 
Provided To Others? Yes  
URL https://www.repository.cam.ac.uk/handle/1810/345488
 
Title Shifting balances in the weighting of sensory modalities are predicted by divergence in brain morphology in incipient species of Heliconius butterflies 
Description Integrating and weighting sensory perception across modalities is crucial to how animals adapt to their environment. Divergence in brain structure is often in sensory processing regions, suggesting that investment reflects ecological needs. Here, we use two parapatric closely related species, Heliconius erato cyrbia and Heliconius himera, to test the hypothesis that divergence in sensory brain regions affects foraging decisions. These butterflies are isolated across an ecological gradient, which is linked to differences in brain morphology, with H. e. cyrbia investing more in visual centres and H. himera investing in olfactory centres. Here, we demonstrate that these two species vary in how they associate visual and olfactory cues with positive food rewards. We found that when individuals were trained on paired olfactory and visual stimuli, then presented with these stimuli in conflict, they showed distinct behavioural responses. Heliconius himera was more likely to favour positive olfactory cues than H. e. cyrbia, which favoured visual cues regardless of the paired stimulus. This suggests that these species have diverged in the emphasis placed on these different sensory domains during foraging, consistent with observed differences in brain morphology. This result strengthens evidence that speciation initiated by local adaptation is partly facilitated by changes in the neural basis of key behavioural functions. 
Type Of Material Database/Collection of data 
Year Produced 2020 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.dbrv15f0h
 
Description Assisted Illustrator Clara Lacy with her 'Natural Creativity: Sex and Trickery' exhibition 
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 I assisted Clara Lacy, a London based illustrator with one of her pieces on mimicry for her 'Natural Creativity: Sex and Trickery' exhibition hosted at the Grant Museum, University College London. My role was to advice on the biology of mimicry, how individuals interact and how this could be portrayed visually. The wider exhibition involved work completed by Clara in collaboration with other researchers, particularly those in Prof. Judith Mank's research Group. The exhibition was open to the general public from 19th October to 23rd December 2016.
Year(s) Of Engagement Activity 2016
 
Description School Visit and Science Festival Project (Swavesey Village College) 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Schools
Results and Impact 15-20 secondary school pupils from Swavesey Village College Science Club attended a presentation and discussion based on my research. I talked about my career in general then focused on aspects of insect brain function and evolution, whilst showing them some images of brain structures from different species. At the end I suggested an experiment the Science Club could perform to test for colour learning in woodlice, the results of which they hope to present at the Cambridge Science Festival. I am continuing to help them refine their protocols and to think through their data.
Year(s) Of Engagement Activity 2017