Genetic architecture and constraint in social evolution

Lead Research Organisation: University of Manchester
Department Name: Life Sciences

Abstract

Although the Darwinian idea of 'survival of the fittest' is central to our understanding of the diversity of life on this planet, the evolution and maintenance of cooperative behaviour remains a conundrum. This is because when cooperating individuals perform some sort of costly act to help one another, they run the risk of disruptive cheaters that do not pay their fair share of the cost. In other words, if cheating is a better strategy, how is cooperative behaviour maintained within populations? In order to better understand this problem, we believe that it will first be important to identify the nature of the genes and pathways that regulate cooperative behaviours. This is because, although evolutionary theory may suggest the best strategy, the genetic changes required may not be possible. For example, some strategies may not exist because any gains may be offset by other fitness costs. Alternatively, the genes and pathways that they regulate behaviour may be organised in such a way that it simply is not be possible for evolution to mould them achieve the optimal or favoured strategy. In this grant, we propose to address each of these problems using a simple system for the study of cooperative behaviour, the soil dwelling social amoeba D. discoideum. Under favourable conditions, D. discoideum amoebae exist as single celled individuals that grow and divide by feeding on bacteria. Upon starvation, however, up to 100,000 amoebae aggregate and cooperate to make a multicellular fruiting body consisting of hardy spores supported by dead stalk cells. Stalk cells thus sacrifice themselves to help the dispersal of spores, raising the question of why selection does not lead to unchecked cheating by individuals that do not pay their fair share of the cost of stalk production. To achieve this goal, we will employ a novel combination of approaches in D. discoideum that allow cooperative behaviour to be analysed with great power. We have recently found that even within a small number different D. discoideum strains, different social strategies could be detected. The work described in this proposal, will allow us to define and classify the number of the strategies within a larger set of strains, because this can be used to determine the number of different 'ways' evolution has allowed social strategies to be modified. We will then ask whether these correspond to distinct molecular or genetic pathways by searching for mutant strains with altered social behaviour. Finally, we will use these data to generate models that will allow us to develop a better theoretical understanding of how cooperative behaviour is maintained and evolutionary outcomes constrained.

Publications

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Description We have discovered that cheating in social limits can be limited by trade offs.

Why slimy cheats don't win


Darwin's evolutionary theory predicts survival of the fittest. So why do different survival tactics co-exist, if evolution should always favour the winning strategy?

To answer that question scientists at the Universities of Bath and Manchester have been studying a single-celled amoeba, also known as slime mould, which displays certain behaviours that have been labelled as "cheating" or "cooperating".

In a study, published in the prestigious journal Current Biology, the team found that cheaters don't necessarily win in terms of overall survival, suggesting that biologists should re-evaluate how they define and measure social cooperation.

Their research has medical implications when it comes to developing therapies that use socially successful bacteria to fight diseases such as lung infections.

Professor Chris Thompson from Manchester's Faculty of Life Sciences explains: "If the cheats always win, then according to Darwin, altruism shouldn't exist. To study this we looked at why the single fittest strategy in the amoeba community doesn't dominate."

The team looked at how amoebae compete against each other during cooperative encounters. These strange microbes generally live in the soil as single cells, eating bacteria, but when food is limited, they clump together to form a 'slug' that moves to a different location before transforming into a fruiting body which eventually releases spores to produce the next generation of amoebae.

Development into a fruiting body requires cooperation, with some of the amoebae forming the stalk part of the fruiting body, effectively sacrificing themselves for the benefit of the ones that become spores. Therefore biologists have labelled the individuals that become the stalk as 'altruists', with the individuals that tend to form lots of spores being identified as 'cheats' because they benefit disproportionately.

However, the scientists from Bath and Manchester found that these assumptions don't necessarily tell the whole story. Those labelled as cheats don't end up having higher success than those that appear to lose since the cheats pay a price for their apparent success by producing larger numbers of lower quality spores. These inferior spores have lower survival rates, so overall the number of spores that survive is similar to those amoebae who 'cooperate'.

Professor Jason Wolf, from the University of Bath's Department of Biology & Biochemistry, explains: "Our study shows that whilst there are definitely winners and losers in social cooperation, you can't measure social success just by counting the number of spores these moulds produce. Those that produce lots of spores often make inferior ones that don't have any overall advantage over their competitors.

"Basically we need to look at the bigger picture when measuring social success, rather than making assumptions based on measuring the wrong things."

Professor Chris Thompson adds: "What our study says is that when we look at systems through just one aspect then that system can appear to be unbalanced and shouldn't work, but in reality we are a collection of many features that together determine our success, and so our variety helps to make us more equal."

He adds: "Our study threw up quite a big surprise because the way we measure fitness in a system is currently misleading. By focussing on the number of offspring (in this case spores) rather than the quality, we're using an incorrect measurement of success.

We have also discovered the existence of a polychromic greenbeard (a demonstration of a Richard Dawkins evolutionary concept)

Fabled cooperation gene discovered in a microbe
Geneticists from the Universities of Manchester and Bath funded by the Wellcome Trust, NERC and the BBSRC are celebrating the discovery of an elusive 'greanbeard' gene that helps explain why organisms are more likely to cooperate with some individuals than others, a problem that has fascinated and puzzled biologists including Darwin.

The renowned evolutionary biologist Richard Dawkins coined the term "greenbeard genes" in his 1976 best seller The Selfish Gene to describe a special type of gene that could solve the conundrum of how organisms identify and direct selfless behaviour to towards other selfless individuals.

The existence of greenbeard genes once seemed implausible, but work published in Nature Communications by the team of geneticists has identified a gene that causes a whole range of 'beard colours' in a social microbe.

These 'slime moulds' live as single celled organisms, but clump together to form a slug like creature when they run out of food. This newly formed slug can move to help them find new sources of food, but this depends on successful cooperation.

The research team found that slime mould cells are able to decide with whom to collaborate. By sequencing their genomes, the research groups discovered that partnership choices are based on a greenbeard gene. This gene encodes a molecule that sits on the surface of a slime mould cell, and is able to bind to the same molecule in another slime mould cell.

This greenbeard gene stands out because it harbours enormous diversity, with most slime mould strains having a unique version of the gene. The team discovered that individuals prefer to partner with those that have similar versions of the gene, and the slugs formed with preferred partners do better than those with non-preferred partners. This demonstrates, according to the team, that there is a whole range 'beard colours' that function to identify compatible partners for cooperation.

Prof Chris Thompson, who led the work at the University of Manchester, said: "Most organisms are social, including microbes. But some individuals are altruistic towards certain individuals and not others. Our discovery of a greenbeard gene goes some way to explaining partner specific cooperative behaviour in slime moulds. And what is especially exciting is the sheer diversity of this gene with every slime mould having its own colour of greenbeard."

He added: "It is certainly more difficult to explain how this might work in humans and other animals.
But ants, for example, are thought to identify each other socially by using a greenbeard pheromone so it's not beyond the realms of possibility that humans may possess something which works along similar lines".

Professor Jason Wolf, from the University of Bath, said: "Dawkins's original greenbeard idea seemed fanciful because it was difficult to imagine a scenario where a region of the genome could have all of the necessary properties. Therefore it was surprising to indentify such a region, and downright astonishing to find that it harboured such a huge array of 'beard colours' that would allow individuals to be very discerning about with whom to cooperate."
Exploitation Route Identifying the genetic basis of trades offs via pleiotropy will be a major challenge. Understanding the extent of other trade offs and how they impact on reducing social cheating will be a challenge
Sectors Education,Other

URL https://thethompsonlab.wordpress.com/
 
Description BBSRC CASE STudentship
Amount £60,000 (GBP)
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 09/2014 
End 09/2018
 
Description BBSRC Project Grant
Amount £500,000 (GBP)
Funding ID BB/M007146/1 
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 03/2016 
End 03/2019
 
Description Biomedical Resource
Amount £498,592 (GBP)
Organisation Wellcome Trust 
Sector Charity/Non Profit
Country United Kingdom
Start 04/2014 
End 04/2017
 
Description Partnership with Syngenta
Amount £35,000 (GBP)
Organisation Syngenta International AG 
Sector Public
Country Global
Start 06/2011 
End 06/2013
 
Title Dictyostelium strains and plasmids 
Description Dictyostelium strains and plasmids which will be used to study P2X receptor function 
Type Of Material Biological samples 
Year Produced 2011 
Provided To Others? Yes  
Impact New ways to think about P2X receptor regulataion 
 
Title Social studies 
Description We developed a new quantitative framework for the analysis of social behaviour 
Type Of Material Model of mechanisms or symptoms - non-mammalian in vivo 
Year Produced 2009 
Provided To Others? Yes  
Impact Paper describing this research was elected to Faculty of 1000 
 
Title Natural strain sequence database 
Description Whole genome sequence from up to 1000 starins 
Type Of Material Database/Collection of data 
Year Produced 2016 
Provided To Others? Yes  
Impact publication of one paper in current biology, and papers to be submitted 
 
Description Baylor college of medicine 
Organisation Baylor College of Medicine
Department Department of Molecular and Human Genetics
Country United States 
Sector Academic/University 
PI Contribution Provision of materials
Collaborator Contribution Advice and expertise on next generation sequencing and bioinformatics
Impact Publications, training
 
Description Brazil partnership 
Organisation Federal University of Sao Carlos
Country Brazil 
Sector Academic/University 
PI Contribution Partnership with Brazilian groups (Sao Paulo) who are sequencing geographically distant species. We have provided the strains for gDNA preparation
Collaborator Contribution Expertise in long read assembly
Impact Multidisciplinary - computational biology and molecular genetics
Start Year 2015
 
Description Studies of social behaviour 
Organisation University of Bath
Country United Kingdom 
Sector Academic/University 
PI Contribution We provided Dictyostelium expertise and socio-biology expertise
Collaborator Contribution They have provided mathematical and theoretical ideas to our socio-biological research
Impact Publication PMID: 19631539 Dissemination: Guardian article, BBC Three Counties Radio interview NERC Project grant NE/H020322/1 awarded July 2010 Publication PMID: 20546090
Start Year 2006
 
Description genetics of socio biology 
Organisation Baylor College of Medicine
Country United States 
Sector Hospitals 
PI Contribution We instigated the project during my time at Baylor College of medicine. The experimental design, conclusions and manuscript preparation were all contributed to by us
Collaborator Contribution New ideas and research directions
Impact PMID: 18272966
 
Description BOLTON SCHOOL 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? Yes
Type Of Presentation Poster Presentation
Geographic Reach Local
Primary Audience Schools
Results and Impact BOLTON SCHOOL PUPIL WORKED IN LAB FOR 6 WEEKS

SCHOOL ASKED TO CONTINUE PLACEMENTS. RESEARCH WAS HIGHLIGHTED TO 6TH FORM STUDENTS THROUGH TALK AND POSTER
Year(s) Of Engagement Activity 2013
 
Description Why am I similar to slime mould? 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Children felt Developmental Biology was interesting from feedback received

Feedback that wanted to do another lab visit next year
Year(s) Of Engagement Activity 2014