NSFDEB-NERC The evolutionary genomics of a major transition in evolution
Lead Research Organisation:
University College London
Department Name: Genetics Evolution and Environment
Abstract
Over 20 years ago, eight major transitions in evolution that explain the emergence of biological complexity were defined, one of which is the evolution of sociality (or superorganismality). Significant advances have been made in understanding the theory underpinning major evolutionary transitions; however, we lack an integrated understanding of the evolutionary patterns and processes of the major transitions. A novel and timely question is whether major transitions arise via gradual or punctuated evolutionary processes. Distinguishing between these is fundamental to our understanding of biological complexity, the natural world and our own origins. We address this question by formulating new a predictive framework on the molecular processes underpinning major transitions, and testing these predictions empirically using multi-level genomic analyses of sociality in 16 species of bees and wasps.
Recent theory on major transitions has extended the concept of the society across levels of biological organization. E.g. genes form a society in protocells, protist cells form a multicellular society, and insects become eusocial superorganisms. A common trait for all societies is the emergence of irreversibly committed phenotypes within the group (e.g. queens and workers in insect colonies; tissue types in multicellular organisms). These analogies are compelling but remain largely conceptual because we do not understand the evolutionary processes by which major transitions (and specifically irreversibility) arise. This is important because the nature of the evolutionary processes shapes the assumptions on which our theoretical understanding is based. Our overarching goal, therefore, is to determine whether the major transition to superorganismality evolved via gradual or punctuated processes, using social insects (the best studied of the major transitions) as a model system.
Until very recently, all studies in social insects assumed that superorganisms evolved via the gradual accumulation of many small changes in molecular processes. However, new conceptual work suggests that the major transition may occur via a less gradual process. This idea proposes that, although many insect species display the hallmarks of 'classic' eusociality, they do not express the specific set of traits that indicate a major transition (i.e. mutual dependency; committed (irreversible) castes). Implicit in this is the assumption that the transition requires a step change in phenotypic traits. A recent empirical analysis of the evolution of sociality in wasps implies a similar pattern, with caste commitment appearing suddenly in (and at the origin of) sociality in wasps. These recent studies raise the intriguing question of whether the major transition to superorganismality is an example of punctuated evolution and not a trait that emerges gradually from many, small micro-evolutionary processes.
In this Proposal we introduce a new framework for dissecting the evolutionary processes of a major evolutionary transition: we identify putative molecular signatures that are likely to typify a gradual or punctuated route to superorganismality. We propose to test these predictions. First, we will generate appropriate multi-layered genomic datasets for 16 species of bees and wasps that span the transition from solitary individuals to superorganisms: these include new genomes, chromosome mapping, new transcriptomes and proteomes. We will then use these datasets to find out which of the evolutionary routes (gradual or punctuated) best explain the transition to superorganismality. Finally, we will bring together experts who share an interest in major transitions across the spectrum of biological organization to discuss the extent to which there are general molecular signatures on the mechanistic basis of a major transition in evolution. If punctuated evolutionary processes are important in driving major transitions, new types of theoretical models will be required.
Recent theory on major transitions has extended the concept of the society across levels of biological organization. E.g. genes form a society in protocells, protist cells form a multicellular society, and insects become eusocial superorganisms. A common trait for all societies is the emergence of irreversibly committed phenotypes within the group (e.g. queens and workers in insect colonies; tissue types in multicellular organisms). These analogies are compelling but remain largely conceptual because we do not understand the evolutionary processes by which major transitions (and specifically irreversibility) arise. This is important because the nature of the evolutionary processes shapes the assumptions on which our theoretical understanding is based. Our overarching goal, therefore, is to determine whether the major transition to superorganismality evolved via gradual or punctuated processes, using social insects (the best studied of the major transitions) as a model system.
Until very recently, all studies in social insects assumed that superorganisms evolved via the gradual accumulation of many small changes in molecular processes. However, new conceptual work suggests that the major transition may occur via a less gradual process. This idea proposes that, although many insect species display the hallmarks of 'classic' eusociality, they do not express the specific set of traits that indicate a major transition (i.e. mutual dependency; committed (irreversible) castes). Implicit in this is the assumption that the transition requires a step change in phenotypic traits. A recent empirical analysis of the evolution of sociality in wasps implies a similar pattern, with caste commitment appearing suddenly in (and at the origin of) sociality in wasps. These recent studies raise the intriguing question of whether the major transition to superorganismality is an example of punctuated evolution and not a trait that emerges gradually from many, small micro-evolutionary processes.
In this Proposal we introduce a new framework for dissecting the evolutionary processes of a major evolutionary transition: we identify putative molecular signatures that are likely to typify a gradual or punctuated route to superorganismality. We propose to test these predictions. First, we will generate appropriate multi-layered genomic datasets for 16 species of bees and wasps that span the transition from solitary individuals to superorganisms: these include new genomes, chromosome mapping, new transcriptomes and proteomes. We will then use these datasets to find out which of the evolutionary routes (gradual or punctuated) best explain the transition to superorganismality. Finally, we will bring together experts who share an interest in major transitions across the spectrum of biological organization to discuss the extent to which there are general molecular signatures on the mechanistic basis of a major transition in evolution. If punctuated evolutionary processes are important in driving major transitions, new types of theoretical models will be required.
Planned Impact
Who will benefit from this research?
This Project will generate important insights into the molecular basis of behaviour, with specific reference to group living in animal societies. 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, and specifically those in the UK and US. 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. The analogies with human societies are particularly compelling for the simple societies of bees and wasps, where individuals have choices on what roles they play. Individuals can be uniquely marked and their behaviours followed: this evokes a special curiosity in the public as the behaviours of individuals can be viewed through the eyes of a 'soap-opera', where individuals can be observed acting in their own interests (selfishness) or go out of their way to help others (altruism).
2) Through an understanding 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 Collaborative 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.
This Project will generate important insights into the molecular basis of behaviour, with specific reference to group living in animal societies. 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, and specifically those in the UK and US. 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. The analogies with human societies are particularly compelling for the simple societies of bees and wasps, where individuals have choices on what roles they play. Individuals can be uniquely marked and their behaviours followed: this evokes a special curiosity in the public as the behaviours of individuals can be viewed through the eyes of a 'soap-opera', where individuals can be observed acting in their own interests (selfishness) or go out of their way to help others (altruism).
2) Through an understanding 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 Collaborative 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
Wyatt CDR
(2023)
Social complexity, life-history and lineage influence the molecular basis of castes in vespid wasps.
in Nature communications
Favreau E
(2023)
Putting hornets on the genomic map
in Scientific Reports
Sumner S
(2023)
Molecular patterns and processes in evolving sociality: lessons from insects
in Philosophical Transactions of the Royal Society B: Biological Sciences
Description | Patterns of genome rearrangements and evolution across bees and wasps in the emergences of social behaviour |
Exploitation Route | Genome sequences and research outcomes will form basis of new grant applications and analyses. |
Sectors | Environment |
Description | Brazilian partners on grant |
Organisation | Sao Paulo State University |
Country | Brazil |
Sector | Academic/University |
PI Contribution | We will provide expertise and training in genome sequencing and bioinformatics. Our contributions will also benefit the wider Brazilian community by generating valuable genomic resources for Brazilian wasp species. |
Collaborator Contribution | Prof Marco Antonio Del Lama will provide expert knowledge on Brazilian solitary wasps, source samples and collect for sequencing. He will also have an instrumental role in interpreting data. |
Impact | This grant only just started and there are no outputs as yet. |
Start Year | 2021 |
Description | Brazilian partners on grant |
Organisation | Universidade de São Paulo |
Country | Brazil |
Sector | Academic/University |
PI Contribution | We will provide training in genome sequencing and bioinformatics to the immediate partner and also the wider Brazilian community through workshops. |
Collaborator Contribution | Prof Fabio Nascimento and his team will provide invaluable local knowledge in sourcing wasps for sequencing and in depth understanding of their natural history. |
Impact | This grant has only just started; samples are being sourced. There are no outputs yet. |
Start Year | 2021 |
Description | A live YouTube session for school children during COVID 19 lockdown |
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 | Schools |
Results and Impact | Lizzy Daly's Earth Live Lessons May 2020: https://www.youtube.com/watch?v=kEjdP4cH63I&list=PL1RC8b7npEWTH3J1GJxa3DWmH-4qpsIjg?dex=11&t=682s I gave a 30 min talk, without any slides, to an online audience; audience members could send questions in. |
Year(s) Of Engagement Activity | 2020 |
URL | https://www.youtube.com/watch?v=kEjdP4cH63I&list=PL1RC8b7npEWTH3J1GJxa3DWmH-4qpsIjg&index=11&t=682s |
Description | An online webinar for the FAO to >1000 agricultural practitioners, academics and policy makers. |
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 | Professional Practitioners |
Results and Impact | Speaker and panellist on Food and Agriculture Organisation of the United Nations (FAO) webinar on Agroecological approaches for Fall Army Worm management (July 2020 - https://bit.ly/32BsOXN; reach: 1199 participants global) |
Year(s) Of Engagement Activity | 2020 |
URL | https://bit.ly/32BsOXN |
Description | Invited article on wasps |
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 | Sumner, S. (2021) Wasps: why I love them, and why you should too. The Conversation. https://theconversation.com/wasps-why-i-love-them-and-why-you-should-too-155982. Second most-read piece of 2021 from University College London academics, read 387,000 times across the Canada, United States, United Kingdom, Luxembourg and Ireland, and republished by The Weather Network, The Raw Story, Phys.org, Delano and InnerSelf. Sumner, S. (2021) Pourquoi les guêpes sont insupportables à la fin de l'été. The Conversation (France). Ninth most-read piece of 2021 from University College London academics, read 146,000 times across the France, Belgium, Canada, Switzerland and United States, and republished by Slate.fr, Ouest-France, Science et Vie, Le HuffPost and HuffPost. |
Year(s) Of Engagement Activity | 2021 |
URL | https://theconversation.com/wasps-why-i-love-them-and-why-you-should-too-155982 |
Description | Invited article on wasps |
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 | Sumner, S (2022) Don't let wasps spoil your jubilee picnic- be like an Argentinian, not like a badger. The Guardian June 4th. https://www.theguardian.com/commentisfree/2022/jun/04/wasps-jubilee-picnic-sting |
Year(s) Of Engagement Activity | 2022 |
URL | https://www.theguardian.com/commentisfree/2022/jun/04/wasps-jubilee-picnic-sting |
Description | Invited article on wasps |
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 | Sumner, S (2022) Scientist tries to take sting out of our fear and loathing of wasps and hails importance to ecosystems Sunday Post 28th June 2022 https://www.sundaypost.com/fp/importance-of-wasps/ |
Year(s) Of Engagement Activity | 2022 |
URL | https://www.sundaypost.com/fp/importance-of-wasps/ |
Description | Invited article on wasps |
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 | Sumner, S (2022) Five facts about the gruesome beauty of solitary wasps. The Conversation May 23rd https://theconversation.com/five-facts-about-the-gruesome-beauty-of-solitary-wasps-183168 |
Year(s) Of Engagement Activity | 2022 |
URL | https://theconversation.com/five-facts-about-the-gruesome-beauty-of-solitary-wasps-183168 |
Description | Invited article on why wasps matter, written from the perspective of a wasp |
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 print and online version of New Internationalist. I received lots of emails and contact over Twitter about this. |
Year(s) Of Engagement Activity | 2021 |
URL | https://newint.org/features/2020/12/07/wasp-biodiversity-why-i-matter |
Description | Online webinar |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Public/other audiences |
Results and Impact | Webinar for a joint invitation from Universiti Kebangsann Malaysia & Entomological Society of Malaysia. |
Year(s) Of Engagement Activity | 2022 |
Description | Online webinar |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Postgraduate students |
Results and Impact | Talk to University of New Brunswick Saint John, Canada (online). Elected by their postgraduates for invited speaker. |
Year(s) Of Engagement Activity | 2022 |
Description | Panel member for an online women in entomology session. |
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 | Royal Entomological Society Women in entomology for National Insect Week June 2020: https://www.youtube.com/watch?v=aJu6fj9xiRU. |
Year(s) Of Engagement Activity | 2020 |
URL | https://www.youtube.com/watch?v=aJu6fj9xiRU |
Description | Publication in Frontiers for Young Minds - journal for 8-16 year olds. On reasons to appreciate wasps. |
Form Of Engagement Activity | A magazine, newsletter or online publication |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Schools |
Results and Impact | https://kids.frontiersin.org/article/10.3389/frym.2019.00149 Sumner S. 2020. Do not swat the wasp! Front. Young Minds. 8:149 |
Year(s) Of Engagement Activity | 2020 |
URL | https://kids.frontiersin.org/article/10.3389/frym.2019.00149 |
Description | Sumner, S. (2020) Why wasps become so annoying at the end of summer. 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 | This article had the second highest reach of any article in August 2020. It was republished in the French version of The Conversation. I received lots of emails about it from around the world, telling me how they had changed their opinion about wasps |
Year(s) Of Engagement Activity | 2020 |
URL | https://theconversation.com/why-wasps-become-so-annoying-at-the-end-of-summer-145053 |