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Final Report Summary - SODOLS (Sociality and division of labour: microbial, behavioural and epigenetic interactions)

Understanding the evolution and maintenance of cooperation is one of the major challenges in biology and is epitomised by the eusocial insects, which Darwin even considered to be potentially fatal to his theory of natural selection. Hamilton’s seminal papers revolutionised our understanding of evolution by explaining cooperation in social insect societies via kin selection, where individuals gain fitness by helping their relatives. But, in the absence of an overarching manager, how is it decided who does what tasks in these cooperative societies? Biological research work often considers individual animals as discrete entities, however they in fact host a plethora of symbiotic microbes that can have significant beneficial or parasitic effects on their hosts. The importance of these symbioses is now beginning to be understood - gut microbiota have been found to affect, and be affected by behaviour and the expression of associated genes in different animals. Gut bacteria and behaviour in social insects are known to be influenced by many of the same factors (e.g. age), however, the relationship between microbial associations, sociality and division of labour, remains almost entirely unexplored. To address this gap, this project investigated the relationship between microbial communities and the evolution of sociality, individual behaviour and division of labour, using two main model systems: the honeybee Apis mellifera, which has complex societies, and the dinosaur ant Dinoponera quadriceps, which has comparably more simple societies.

Description of work performed

Intensive behavioural observations of honey bee colonies (highly social) have been completed, where each experimental colony was set up with same-aged workers that were individually marked. Similarly, behavioural observations of dinosaur ant colonies (“primitively” social) have been completed. This behavioural work has been extended by examining the relationship between landscape exposure and honey bee and bumblebee microbial communities. Honey bee colonies were exposed to common land use types, and in a second experiment, 40 bumblebee colonies were exposed to field realistic stressors (including commonly used pesticides, fungicides and parasites) under laboratory conditions. Bumblebees have a similar core microbial community to honey bees and therefore provide a useful laboratory model.

Community amplicon sequencing (Illumina, MiSeq) was used to characterise and compare (within each of the different behavioural and environmental exposure experiments) the gut microbial community of different behavioural castes, and of bees exposed to different broad environments and key environmental parameters. A bioinformatics pipeline (LotuS) was used for amplicon sequence processing in all experiments, and statistical analyses and comparisons of microbial communities were conducted using LotuS outputs.

Main results achieved

Honey bee workers (where age is controlled for) performing different behavioural tasks were found to exhibit significant differences in the abundance of some core bacterial community taxa. Workers performing predominantly in nest (nursing and food processing) versus foraging behaviours showed a higher abundance of the bacterial taxa Lactobacillus and Bifidobacterium, both of which have been reported elsewhere to be associated with processing complex carbohydrates and maintaining bee health. These differentially represented bacteria identified are key candidates for functional analyses including full metagenome sequencing studies. In an insect with a comparatively more simple society, dinosaur ants, the relative abundance of some gut bacterial taxa was also found to be different depending on the behaviour performed (in nest versus outside behaviours), the latter results are currently being finalised.

Further the broad environment that bees are exposed to was found to influence the relative abundance of some members of their microbial community. This includes known core taxa thought to have functions in nutrition and health, with some taxa being similar to those identified in our bee behavioural analyses (including a Lactobacillus species, and an Alphaproteobacteria species Bartonella apis, recently reported to encode genes involved in the degradation of plant secondary metabolites). Further, in controlled laboratory experiments bumblebees exposed to different combinations of field realistic stressors were found to show significant differences in the relative abundance of core microbial taxa, including some taxa found to differ in bees exposed to different landscape types.

Expected final results and potential impact and use

The results gained in this project emphasise the complexity of the relationship between the host, its gut bacteria, behaviour and the environment. While previous studies have delineated a characteristic dominant set of bacteria inhabiting the honey bee gut, here we provide evidence that the behavioural tasks that bees perform (and therefore their immediate local environment), and the broad environment that bees are exposed to, influences the relative abundance of some members of that microbial community. This includes known core taxa previously reported to have functions in nutrition and health. Additionally, our lab based study where bumblebees were exposed to field realistic stressors, identifies the likely parameters (pesticides, fungicides and parasites) driving the differences in bacterial communities seen in bees exposed to different broad landscape types. Further, our results so far show that less complex societies than the highly social honey bees, exemplified in our study by the dinosaur ants, also exhibit differences in their microbial community depending on behaviour, where the local environment is held constant (inside and outside the nest under laboratory conditions). Under an added research objective, currently nearing completion, we will gain results of how other key interrelated parameters (altitude and environment) affect sociality and morphology in a socially polymorphic species (the sweat bee Lasioglossum calceatum).

The differentially represented gut bacteria identified in this study are candidates for further functional analyses. Key next steps will be to test the bacteria taxa identified here for their function in behavioural division of labour, and also in the host’s ability to deal with exposure to different environments, highly interconnected facets in insect societies. This means the different angles of this study highlight a potential feedback loop where environmental exposure (e.g. when performing in nest versus tasks outside the nest) influences bacterial community, and bacterial community in turn influences host health and also influences or maintains behavioural task, which in turn feeds back into environmental exposure.

Related information

Reported by

UNIVERSITY OF SUSSEX
United Kingdom
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