The molecular basis of phenotypic transitions in eusocial evolution

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

Abstract

Major evolutionary transitions are key sources of diversity in the natural world. Yet we understand little about the mechanisms by which they arise, and specifically their molecular basis. An outstanding question is to what extent do these transitions arise via decoupling of ancestral genes and traits, or the evolution of new genomic material for new traits. This is important as it tells us whether molecular mechanisms constrain major evolutionary change. This project aims to explore the molecular basis a major evolutionary transition.
The evolution of sociality is one of eight major evolutionary transitions and examples can be found across levels of biological organisation: genes aggregate into genomes, cells into multicellular organisms, and insects into societies. In each case, smaller entities unite to form larger higher-level entities, with division of labour, cooperation and specialized roles. In the transition to sociality the ancestral traits of reproduction and non-reproductive tasks, are thought to be decoupled to form a division of labour among group members. For example, in the transition from single- to multi-cellularity, cells become specialised as reproductive (gametes) or non-reproductive (somatic) units; in the transition from solitary living to sociality in insects, individuals become specialised as egg-layers (queens) or provisioners (workers). The decoupling of ancestral traits to form social traits is the main hypothesis to explain the mechanism by which sociality evolves.
However, the decoupling hypothesis fails to consider the evolution of new behaviours or traits that arise during major transitions. These include: (1) the evolution of group living from a solitary, ancestral state; (2) the evolution of altruistic behaviour from an ancestral, selfish behaviour; (3) the evolution of inflexible (committed) phenotypes, from flexible (uncommitted) phenotypes. Therefore, defining the transition to sociality simply as a re-organisation of ancestral reproductive and provisioning traits maybe too simplistic, as it does not account for the emergence of essential novel traits.
This Project will identify the genes and proteins underlying the decoupling of ancestral traits (reproduction and provisioning) and novel social traits (group living, altruism and committed castes) in the eusocial wasps. Eusocial insects are powerful models for studying the mechanisms and evolution of sociality. The eusocial wasps include species representatives across the spectrum of social complexity from species that can choose whether to be social or not, to highly complex, committed societies with extreme task specialists and complex societies.
We will generate genome sequences and interrogate phenotype-specific transcriptomes and proteomes for 5 species of eusocial wasps. This work will be the first systematic interrogation of the molecular basis of insect behaviours across the spectrum of social diversity. We combine field manipulation experiments with state-of-the art genomic and bioinformatic approaches to dissect social behavior in an ecologically relevant context. The Work Programme consists of 3 stand-alone species-level studies on wasps representing different stages in social evolution. We use field manipulation experiments as a 'top-down' way of identifying genes associated with each behavioural innovation. Then, we exploit the datasets generated by these studies to address comparative questions on the molecular basis of social evolution. The combination of transcriptomics and proteomics is a powerful yet little exploited approach that is likely to lead to significant scientific breakthroughs. Our approach, therefore, seeks to uncover proximate mechanisms underlying key innovations in social behaviour in order to address ultimate questions on the nature of this major transition in evolution.

Planned Impact

Who will benefit from this research?
This Project will generate important insights into the molecular basis of behaviour, with specific reference to social behaviour. The outcomes are therefore of a fundamental, 'blue-skies' nature, generating basic information on the building blocks of the natural world, using a charismatic and ecologically important group of organisms. Apart from academic beneficiaries, the main beneficiaries will be the general public. Public understanding of science is essential for the future of our societies and economies.
How will they benefit from this research?
1) Through an understanding the science behind their own social behaviour
People are intrinsically interested in their own actions and behaviors. Social insect societies have many parallels with our own, and social insect research provides a tractable dialogue with the public and the theory and mechanisms of social behaviour. For example, social insects resolve conflicts with neighbours and use division of labour to enhance social group performance and cohesion. Human societies are driven by division of labour, in both our work places and homes. Wasp societies, where individuals can be uniquely marked and their behaviours followed, evoke a special curioristy in the public as the wasps can be viewed through the eyes of a 'soap-opera', where individuals cane be observed acting in their own interests (selfishness) or go out of their way to help others (altruism).
2) Through an understanding of how their behaviours are products of their genomes.
The general public broadly understands genetic inheritance (e.g. in disease etc), but the interaction between genes and the environment, and how a genomes' responsiveness determines adaptation and plasticity at the whole organism level, remains less well appreciated by the public. An education of how behavior is not 'hardwired' and that the environment can affect how your genes behave has important health and societal consequences for the general public.
3) By learning about the diversity of social insects and how they came to be
The public are exposed regularly to stories about beneficial bees, invading ants and killer wasps in the media these days. This results in most social insects (with the exception of bees) being viewed as pests, unimportant and undesirable. Yet, wasps and ants (as well as bees) are vital components of global ecosystems as pest controllers, pollinators, seed dispersers and decomposers. The public will benefit from a more balanced education of the diversity of social insects that can be found, how this diversity evolves and the importance to our planet.
4) Through an understanding of the importance inter-disciplinary collaborations in modern-day science
The general public have a pre-conceived idea of what a modern scientist does, specifically that scientists are insular creatures who live in labs with expensive equipment, and that their science is somewhat detached from the real world. The public would benefit from the chance to understand how modern science is highly inter-disciplinary, and that science progresses best when scientists from different skill sets interact and share ideas. Our Project will benefit the public as it is an explicit example of how 'welly boot' science can be married with computational science and molecular biology to advance our understanding of the natural world.

Publications

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Cini A (2019) Inquiline social parasites as tools to unlock the secrets of insect sociality. in Philosophical transactions of the Royal Society of London. Series B, Biological sciences

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Toth AL (2016) Patterns of longevity across a sociality gradient in vespid wasps. in Current opinion in insect science

Related Projects

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NE/M012913/1 01/05/2015 16/10/2016 £675,317
NE/M012913/2 Transfer NE/M012913/1 17/10/2016 31/05/2020 £498,530
 
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Description Conacyt studentship
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Description Article in Countryfile Magazine 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Commissioned article in Countryfile Magazine about wasps.
Year(s) Of Engagement Activity 2018
 
Description Interview on The One Show, about social wasps 
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 Invited expert to talk about social wasps and their importance. The programme aimed to challenge the public's view of 'unpopular animals'.
Aired at 6pm on BBC1
Year(s) Of Engagement Activity 2016
URL http://www.bbc.co.uk/programmes/p049f9js
 
Description Sumner S & Brock R (2016) In defence of wasps. The Conversation. 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Invited article for The conversation on the ecosystem value of wasps. The article was then re-published multiiple times, globally. eg.
http://www.independent.co.uk/environment/in-defence-of-wasps-why-squashing-them-comes-with-a-sting-in-the-tale-a7144306.html
Year(s) Of Engagement Activity 2016
URL http://theconversation.com/in-defence-of-wasps-why-squashing-them-comes-with-a-sting-in-the-tale-607...
 
Description Sumner, S. & Brock R. 2016. "Social Wasps: No ASBO Required." Professional Pest Controller Magazine. 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Invited article on the importance of wasps as predators of arthropods.
Year(s) Of Engagement Activity 2016
URL http://www.bpca.org.uk/pages/index.cfm?page_id=59
 
Description Wasps - The Neglected Darlings of the insect world 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Public lecture at ZSL.
Year(s) Of Engagement Activity 2018
URL https://www.zsl.org/science/whats-on/wasps-the-neglected-darlings-of-the-insect-world-and-conservati...