Understanding major transitions in individuality

Lead Research Organisation: University of St Andrews
Department Name: Biology

Abstract

Major transitions in individuality occur when a group of separate organisms evolves into a higher-level organism in its own right. For example, the ancestors of the social insects used to live a solitary existence, but today they form highly elaborate, cooperative societies that can be considered "superorganisms" in their own right. Current theory describing major transitions in individuality highlights the importance of clonal reproduction and systems of policing in maintaining the integrity of the superorganism. However, the social insects appear to have evolved a higher level of individuality on the basis of strict lifetime monogamy, which has abolished conflicts of interest within the colony. I will develop new theory to incorporate this monogamy hypothesis into the theory of major transitions in individuality, and I will investigate how the quirky genetics of some species can lead to other forms of conflict arising within their societies.

Planned Impact

The successful media coverage of my previous work on social evolution has demonstrated that the general public has a profound interest in this topic, so they stand to benefit from the research in this respect. In general, the public are interested in evolution, because we are all interested in our origins. Social evolution is of particular interest, because it illuminates our social origins, and the reasons for love and strife within families. The British public also take a special interest in natural history, including the alien biology of the insect world.

Of more applied interest, my research may eventually inform agricultural practice and policy. The social insects are of enormous economic significance: for example, the honeybee is responsible for much pollination of crop plants. Understanding the factors that maintain the integrity of the colony may help protect bee colonies from collapse due to pressure from social parasites. My work on arbuscular mycorrhizal fungi and their mutualism with plant roots may lead to the development of new cultivation techniques to maximize crop productivity. Although I will not be directly developing new agricultural methodology in this research, my collaborative partnership with Dr Kiers -- who does interact closely with farmers -- will ensure that such insights are carried through to novel agricultural technology.

Publications

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Alpedrinha J (2014) Haplodiploidy and the evolution of eusociality: worker revolution. in The American naturalist

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Davies NG (2018) Monogamy promotes altruistic sterility in insect societies. in Royal Society open science

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Dyble M (2018) Inclusive fitness for in-laws. in Biology letters

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Faria GS (2017) Sexual selection modulates genetic conflicts and patterns of genomic imprinting. in Evolution; international journal of organic evolution

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Faria GS (2015) Sex-biased dispersal, kin selection and the evolution of sexual conflict. in Journal of evolutionary biology

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Farrell EJ (2015) Intragenomic Conflict over Dispersal. in The American naturalist

 
Description 1. I have developed a theory of multi-level selection for application to class-structured populations. Published in Journal of Evolutionary Biology.

2. I have developed a general model of the evolution of genome elimination (including paternal genome elimination, an important form of male haploidy) under inbreeding, XY/XO/ZW/ZO sex determination, zygotic/maternal/paternal effects, autosomal or sex-chromosomal inheritance, and imprinted versus unimprinted gene expression. This work has explained why, across 1000s of animal species, genome expression typically occurs under male heterogamety, under inbreeding and in the form of elimination of the paternal genome. Published in Ecology Letters.

3. To facilitate my investigation of the interplay between kin selection and male haploidy, I have proven the crucial mathematical result that, collectively, juvenile females have twice the reproductive value of juvenile males in male haploid populations, even though, collectively, the total reproductive value of all females need not be twice that of all males, in the context of age-structure. Published in Journal of Theoretical Biology.

4. I have developed theory for genomic imprinting conflict to explain the observed imprinting of gene Grb10 in mouse pups and their mothers' mammary tissue, showing that this pattern of gene expression may be driven by a conflict of interest between paternal-origin genes versus maternal-origin genes in both pups and their mothers. Published in PLOS Biology.

5. I have provided formal mathematical support for key features of the analogy of 'biological markets' as applied to plant-mycorrhizal interactions and demonstrated its theoretical connections with evolutionary game theory. Published in Evolution.

6. I have reviewed and synthesised research on the topic of the major transitions in individuality. Published in Proceedings of the National Academy of Sciences, USA.

7. I have developed theory showing that two celebrated sex-ratio invariant results, concerning constancy in the number of males with respect to variation in dispersal rate or variance in fecundity, break down when both sources of variation are occurring simultaneously. Published in Proceedings B.

8. I have further developed the theory of multi-level selection in class-structured populations, with reference to the Price-Hamilton versus contextual-analysis approaches to multi-level selection. Published in Journal of Evolutionary Biology.

9. I have developed theory on individual-level and group-level adaptation in social spiders. Published in Nature.

10. I have developed theory on intragenomic conflict with regard to whether or not the individual should engage in dispersal behaviour, from which I have derived testable predictions concerning patterns of genomic imprinting of genes underpinning dispersal phenotypes. Published in American Naturalist.

11. I have developed theory showing that mutualistic partners may be favoured to harm each other in order to stabilise the mutualism, with particular application to plant-mycorrhizal interactions. Published in Nature Communications.

12. I have developed theory investigating the consequences of kin selection on the evolution of sexual-conflict behaviours. Published in Journal of Evolutionary Biology.

13. I have developed theory demonstrating an invariant result for the evolution of dispersal, whereby each mother produces the same number of non-dispersing offspring irrespective of variation in the total number of offspring produced by each mother. Published in Journal of Evolutionary Biology.

14. I have developed theory demonstrating that a 'loner' strategy can stabilise bacterial cooperation and ecological diversity, and have confirmed the predictions of this theory using evolutionary experiments with the opportunities human pathogen Pseudomonas aeruginosa. Published in Proceedings B.

15. I have developed theory demonstrating the potential existence of intragenomic conflict with regard to soldiering behaviour in polyembryonic parasitoid wasps, deriving testable predictions concerning patterns of genomic imprinting that may allow discrimination between competing hypotheses as to these soldiers' primary function. To be published in American Naturalist.

16. I have synthesised theory and recent recent research findings concerning the bizarre female biased sex ratios of quasi social parasitoid wasps, pointing out directions for future research. To be published in a special issue of Entomologia Experimentalis et Applicata.

17. I have developed theory showing that sex-biased dispersal can drive intragenomic conflict and genomic imprinting in relation to sexual conflict phenotypes. To be published in Evolution.

18. I have developed theory showing that sex-biased dispersal can drive intrafamily and intragenomic conflict in relation to human warfare, yielding predictions for corresponding patterns of genomic imprinting and associated human behavioural disorders. To be published in Proceedings of the Royal Society of London B.

19. I have developed theory showing the interplay between sex allocation and the evolution of sib-altruism, pointing to a key role for the ecology of sex in driving patterns of sociality in arthropods. Published in Ecology Letters.

20. I have reviewed misconceptions on the application of the theory of biological markets to plant-fungus symbioses. Published in Nature Plants.
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21. I have developed and analysed models of viral "germline" investment in the context of chronic viral infections. Published in Trends in Microbiology.

22. I have developed a formal and fully comprehensive theory of intragenomic conflict. Published in Nature Ecology & Evolution.

23. I have discussed the rationale and formal underpinnings of optimality / adaptationist approaches in evolutionary biology. Published in Interface Focus.

24. I have developed and analysed models of intragroup and intragenomic conflict in relation to anti-predator chemical defence in insects, yielding predictions that may facilitate gene discovery in relation to agriculturally important products. To be published in Ecology and Evolution.

25. I have developed theory showing how the effect of infraspecific relatedness on the evolution of public goods cooperation is diminished in the context of multi species communities. Published in Evolution.

26. I have developed theory showing that male-only warfare may evolve even when there are no underlying sex differences in ecology, owing to positive feedbacks that are able to magnify even chance differences that arise between the sexes. Published in Proceedings B.

27. I have developed theory on human brain evolution suggesting that ecological challenges rather than social challenges better explain why humans have evolved large brains. Published in Nature.

28. I have provided an overview and synthesis of the theory of group selection. Published in Oxford Bibliographies in Evolutionary Biology.

29. I have developed theory showing the formal link between R. A. Fisher's "sexy son effect" in the sexual selection literature, on the one hand, and W. D. Hamilton's "greenbeard effect" in the kin selection literature, on the other hand. Published in Evolution Letters.

30. I have developed theory on the application of kin selection to social interaction among affinal kin. Published in Biology Letters.

31. I have developed theory showing that female monogamy is a robust promoter of altruistic sterility in insect societies. Published in Royal Society Open Science.

32. I have reviewed and synthesised the evolutionary literature on the link between dispersal and genomic imprinting. Published in Current Opinion in Behavioural Science.

33. I have developed theory on the social evolutionary drivers of sleep, with a focus on sex differences, intragenomic conflicts and sleep disorders / pathologies. Published in Proceedings B.

34. I have developed theory on the evolution of haplodiploidy, determining under which sex determination mechanisms a haploid offspring developing from an unfertilised egg is expected to be male, and showing that inbreeding does not impede the evolutionary invasion of male haploidy as had previously been thought. Published in Evolution Letters.
Exploitation Route Several of the contributions made so far have been methodological, and will enable me to conduct the more applied parts of the research proposal. They will, however, be useful for other researchers pursuing other research topics. Moreover, even for these primarily methodological contributions, I have developed novel theoretical predictions that empirical researchers may now go on to test as part of their own research programmes.
Sectors Agriculture, Food and Drink,Communities and Social Services/Policy,Environment,Healthcare,Government, Democracy and Justice,Pharmaceuticals and Medical Biotechnology

URL http://synergy.st-andrews.ac.uk/gardner/
 
Description Consolidator Grant
Amount € 1,968,688 (EUR)
Funding ID 771387 
Organisation European Research Council (ERC) 
Sector Public
Country European Union (EU)
Start 05/2018 
End 04/2023
 
Description John Templeton Foundation
Amount £130,779 (GBP)
Organisation The John Templeton Foundation 
Sector Academic/University
Country United States
Start 06/2017 
End 05/2019
 
Description Marie Sklodowska-Curie Fellowship
Amount £130,303 (GBP)
Organisation European Commission 
Sector Public
Country European Union (EU)
Start 10/2016 
End 09/2018
 
Description Newton Fellowship
Amount £92,550 (GBP)
Organisation The Royal Society 
Sector Academic/University
Country United Kingdom
Start 01/2017 
End 12/2018
 
Title Complete Numerical Solutions For "Inference Of Ecological And Social Drivers Of Human Brain-Size Evolution" By Mauricio González-Forero And Andy Gardner 
Description This zip file contains the complete numerical solutions across the parameter sweep over the P parameters for the six cases considered. /1RatioForm/ -> solutions for power competence.
/2DiffForm/ -> solutions for exponential competence. /1RatioForm/1BenchmarkFromSimpleInitialGuess -> solution for the step 1 of initialization (section 5 of the SI).
/1RatioForm/2Benchmark/ -> solution for the step 2 of the initialization (section 5 of the SI).
/1RatioForm/3AdditiveCoop/ -> solutions across the P parameter combinations for additive cooperation.
/1RatioForm/4MultCoop/ -> solutions across the P parameter combinations for multiplicative cooperation.
/1RatioForm/5SubMultCoop/ -> solutions across the P parameter combinations for submultiplicative cooperation. The contents of /2DiffForm/ are analogous. The P vector is written in these files in the order (etas,etac,etaC,etag), where
etas -> P1
etac -> P3
etaC -> P2
etag -> P4 The files 1runNotesACMC.pdf and 2runNotesSC.pdf contain the tree structure of the parameter sweep, specifying which parameter combination was used as the resident and which combinations converged to an uninvadable strategy (those with a checkmark). The file 3runNotesMaternalCareOptimization.pdf contains the 10 parameter combinations that yielded the best adult fit, which then were subject to variation in the parameter phi to find the combination that yielded the best ontogenetic fit. The file 4runNotesDuplicates.pdf gives the parameter combinations that were not run because they are equivalent to other parameter combinations. Running [T,N1,run,Tshort,N1short,runShort]=etaCombinations in Matlab and typing run.seed{i}.parallel{:} gives the "next" parameter combinations from parameter combination i (where i is a number 1,2,...) for PC-AC, EC-MC, PC-SC, and EC-SC. The meaning of "next" is explained in step 4 of the parameter sweep (section 5 of the SI). Typing runShort.seed{i}.parallel{:} gives the "next" parameter combinations from parameter combination i for PC-MC and EC-AC. The terminal folders contain the solutions and have the following files:
brainNashDeep.m -> the master file launching the iteration of best responses.
brainMainDeep.m -> the file launching one iteration solving the optimal control problem to find best response.
brainMainTestRunDeep.m -> runs a test to check if there are infeasibility warnings.
brainContinuous.m -> specifies the dynamic constraints.
brainEndpoint.m -> specifies the terminal constraints.
parameters.m -> specifies the parameter values and rescales them to rescale units as specified in section 5 of the SI.
getSolution.m -> extracts solution.
plots.m -> plots solutions over best response iterations.
brainPlot.m -> plots solution of a given best response iteration.
guessDeep.mat -> initial guess and resident used.
solutionNashDeep.mat -> solutions over best response iterations.
solutionDeep.mat -> solution of last best response iteration.   
Type Of Material Database/Collection of data 
Year Produced 2018 
Provided To Others? Yes  
 
Title Data from: Monogamy promotes altruistic sterility in insect societies 
Description  
Type Of Material Database/Collection of data 
Year Produced 2018 
Provided To Others? Yes  
 
Description Alberto Micheletti & Graeme Ruxton 
Organisation University of St Andrews
Department Earth & Environmental Sciences
Country United Kingdom 
Sector Academic/University 
PI Contribution PhD supervision, project formulation, mathematical modelling, paper writing.
Collaborator Contribution PhD supervision, project formulation, mathematical modelling, paper writing.
Impact Micheletti AJC, Ruxton GD & Gardner A (in press) Intrafamily and intragenomic conflicts in human warfare. Proceedings of the Royal Society of London Series B - Biological Sciences.
Start Year 2015
 
Description Antonio Rodrigues 
Organisation University of Cambridge
Country United Kingdom 
Sector Academic/University 
PI Contribution Co-authored papers
Collaborator Contribution Co-authored papers
Impact Rodrigues AMM & Gardner A (2016) The constant philopater hypothesis: a new life history invariant for dispersal evolution. Journal of Evolutionary Biology 29, 153-166. Rodrigues AMM & Gardner A (2015) Simultaneous failure of two sex-allocation invariants: implications for sex-ratio variation within and between populations. Proceedings of the Royal Society of London Series B - Biological Sciences 282, 20150570.
Start Year 2014
 
Description Erica Kiers, Stuart West, Gregory Wyatt, Heike Bücking, Gijsbert Werner 
Organisation Free University of Amsterdam
Country Netherlands 
Sector Academic/University 
PI Contribution paper writing
Collaborator Contribution paper writing
Impact Kiers ET, West SA, Wyatt GAK, Gardner A, Bücking H & Werner G (2016) Misconceptions on the application of biological market theory to the mycorrhizal symbiosis. Nature Plants 2, 16063.
Start Year 2016
 
Description Francisco Ubeda 
Organisation Royal Holloway, University of London
Country United Kingdom 
Sector Academic/University 
PI Contribution Mathematical modelling & paper writing
Collaborator Contribution Mathematical modelling & paper writing
Impact Úbeda F & Gardner A (in press) Mother and offspring in conflict: why not? PLoS Biology.
Start Year 2014
 
Description Ian Hardy and colleagues 
Organisation University of Nottingham
Country United Kingdom 
Sector Academic/University 
PI Contribution Co-authored paper
Collaborator Contribution Co-authored paper
Impact Kapranas A, Hardy ICW, Tang X, Gardner A & Li B (in press) Sex ratios, virginity and local resource enhancement in a quasisocial parasitoid. Entomologia Experimentalis et Applicata.
Start Year 2015
 
Description Laura Ross 
Organisation University of Edinburgh
Country United Kingdom 
Sector Academic/University 
PI Contribution Mathematical modelling & paper writing
Collaborator Contribution Paper writing
Impact Gardner A & Ross L (in press) Mating ecology explains patterns of genome elimination. Ecology Letters.
Start Year 2014
 
Description Lythgoe and colleagues 
Organisation University of Oxford
Country United Kingdom 
Sector Academic/University 
PI Contribution Developing and analysing mathematical models of viral "germline" optimal investment in the context of chronic viral infections.
Collaborator Contribution Provided framing of these mathematical results in their biological context.
Impact Lythgoe KA, Gardner A, Pybus OG & Grove J (2017) Short-sighted virus evolution and a germline hypothesis for chronic viral infections. Trends in Microbiology 25, 336-348.
Start Year 2016
 
Description Petri Rautiala 
Organisation University of Jyvaskyla
Country Finland 
Sector Academic/University 
PI Contribution Co-authored paper
Collaborator Contribution Co-authored paper
Impact Rautiala P & Gardner A (in press) Intragenomic conflict over soldier allocation in polyembryonic parasitoid wasps. American Naturalist.
Start Year 2015
 
Description Rolf Kuemmerli & colleagues 
Organisation University of Zurich
Country Switzerland 
Sector Academic/University 
PI Contribution Co-authored paper
Collaborator Contribution Co-authored paper
Impact Inglis RF, Biernaskie JM, Gardner A & Kümmerli R (2016) Presence of a loner strain maintains cooperation and diversity in well-mixed bacterial communities. Proceedings of the Royal Society of London Series B - Biological Sciences 283, 20152682.
Start Year 2014
 
Description Silvia Paracchini 
Organisation University of St Andrews
Country United Kingdom 
Sector Academic/University 
PI Contribution Co-supervision of PhD project (60%) on genomic imprinting analysis.
Collaborator Contribution Co-supervision of PhD project (30%) on genomic imprinting analysis.
Impact None at this time.
Start Year 2017
 
Description Susana Varela 
Organisation University of Lisbon
Country Portugal 
Sector Academic/University 
PI Contribution Co-supervision of PhD student
Collaborator Contribution Co-supervision of PhD student
Impact Faria GS, Varela SAM & Gardner A (2015) Sex-biased dispersal, kin selection and the evolution of sexual conflict. Journal of Evolutionary Biology 28, 1901-1910.
Start Year 2015
 
Title Computer Code For "Inference Of Ecological And Social Drivers Of Human Brain-Size Evolution" 
Description This software performs the numerical solutions and produces the parameter-sweep figures for the paper "Inference of ecological and social drivers of human brain-size evolution", by Mauricio González-Forero and Andy Gardner. 
Type Of Technology Software 
Year Produced 2018