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Division of Labour and the Evolution of Complexity

Periodic Reporting for period 3 - Division (Division of Labour and the Evolution of Complexity)

Période du rapport: 2023-01-01 au 2024-06-30

Division of labour is fundamental to the evolution of life on earth, allowing genes to work together to form genomes, cells to build organisms, pathogens to escape immune attack, and eusocial insect societies to achieve ecological dominance. Consequently, if we want to understand how life on earth evolved, we need to understand why division of labour does or, just as importantly, does not evolve.

There are two major outstanding problems for our understanding of division of labour:

First, how can we explain why division of labour has evolved with some traits, in some species, but not others? Given the potential benefits of dividing labour, why does it not arise more frequently in cooperative species?

Second, in cases where division of labour has evolved, how can we explain the form that it takes? Why do factors such as the degree of specialisation, or mechanism used to produce different phenotypes, vary across species?

I will combine my social evolution expertise with novel synthetic and genomic approaches to address these problems.

I will explain the distribution and form of division of labour in the natural world, with an interdisciplinary research programme, divided into four work packages:
(1) I will provide the first experimental test of the fundamental assumption that division of labour provides an efficiency benefit, by synthetically manipulating bacteria.
(2) I will test how selection has acted for and against the evolution of division of labour in natural populations of bacteria, using novel genomic analysis techniques.
(3) I will determine why division of labour evolved in some species, but not others, with an across species study on insects, and experimental evolution of bacteria.
(4) I will establish a new field of research on why different species use different mechanisms to divide labour: genetic differences, environmental cues, or random assignment of roles. I will develop theory to explain this variation, and test this theory experimentally with bacteria.
We have made good progress. Although, the complications created by the COVID pandemic delayed some things, aand slowed progress in some areas – consequently, we had to rearrange our priorities for this period.
Work Package 1. The start date of this package was delayed, due to the post-doc not be able to start, and then limited lab availability. The post-doc (Zhang) started at month 13, not the planned month 1. In addition, limited lab availability has slowed his work until restrictions were recently relaxed. Nonetheless, Zhang has started engineering of strains. It has proved harder to engineer (construct) the strains for work package 1 than we had envisaged. Possibly due to complications arising from their placement on a plasmid. We are trying different ways to get around this. To make up for the delay in the start of the empirical part of this objective, we extended our theoretical work, to examine how to test for different factors which may favour division of labour (Cooper et al. Submitted eLife).
Work Package 2. This package was started early, due to the fact that this is a computer based project, and so could be started during lockdown. The postdoc (Belcher) started at month 7, not 13. We have also just hired another post-doc (Dewar), and obtained an independently funded PhD student to work in this area (Hao). Our genomic analyses started well, and we have already shown that putatively social traits show relaxed selection (Belcher et al. 2022PNAS), and are not more represented on plasmids (Dewar et al. 2021 Nature Ecology & Evolution). We are expanding the population genetic analyses to look at different species; analysing gene connectivity and core versus accessory genome, to test how they relate to sociality.
Work Package 3. We started collection of the insect database early, because this work could be carried out during lockdown. We hired a research assistant (Turner) for two 3 month periods to collect data from the literature, alongside a PhD student funded by Oxford University (Bell-Roberts), and have also funded a PhD student (Turner, started October 2022). We have also hired dos Santos at 805 time for 12 months to carry out targeted development of theoretical models. We found that colony size and queen mating frequency are the main determinants of division of labour in ants. Similar patterns hold when examining either: (a) the number of castes (Bell-Roberts et al. In prep); or (b) morphological differentiation between queens and workers (Turner et al. In prep). We also complemented this work with: (a) a comparative analysis of cooperation in public goods experiments in humans (Burton-Chellew & West 2021 Nature Human Behaviour); (b) a comparative analysis of division of labour between symbionts and their hosts (Cornwallis et al Submitted); (c) analogous work on viruses, reviewing phenotypic diversity and cheating (Leeks et al. 2021 Nature Communications), and showing that selection for cheating can lead to segmented viruses (Leeks et al. In prep); (d) showing theoretically how environmental variation influences selection for altruistic division of labour (dos Santos et al. In prep).
Work Package 4. The planned theoretical work started on time, hiring a post-doc (Scott). We also acquired a PhD student to work in this area, funded by Taiwan Scholarship / Oxford University (Liu). We have already completed an analysis of comparing the evolution of two mechanisms for division of labour: random versus coordinated (Cooper et al. 2022 Nature Communications; Liu et al. 2021 Ecology & Evolution). We have also expanded work in this area theoretically, to examine when genetic kin discrimination can be used to stabilise altruistic division of labour (Scott et al. 2022 Nature Communications).
Overview: We have also reviewed the general area (West et al. 2021 Nature Ecology & Evolution).
Our published work has made significant breakthroughs, beyond the state of the art, and opened up new areas of research. This has included: (a) providing convincing evidence for cooperation in a natural population of bacteria, and opened up a whole new apploication of population genetics (Belcher Belcher et al. 2022 PNAS); (b) defined a new problem, and theoretically evaluated a novel hypothesis, that now needs to be tested empirically (Cooper et al. 2022 Nature Communications; Liu et al. 2021 Ecology & Evolution); (c) providing a solution to an existing paradox, and showed how genetic kin recognition can be evolutionarily stable (Scott et al. 2022 Nature Communications); (d) combined theory and data to show decisively that horizontal gene transfer does not favour cooperation, as had been previously argued, while also showing the importance of carrying out comparative genomic analyses while controlling for phylogeny (Dewar et al. 2021 Nature Ecology & Evolution); (e) significantly advancing the research field by synthesising the existing literature in ways that provided conceptual overview, and clarified the major outstanding challenges (West et al. 2021 Nature Ecology & Evolution).