Evolutionary deconstrcution of C. elegans aggregation behaviour : environmental and genetic correlates of aggregation behaviour and its individual and interaction components

Abstract

Studies of animal behaviour have increasingly expanded its focus towards the evolutionary explanations behind various behaviours. Albeit the challenges in conceptualisation, some evolutionary models have successfully inferred the ontogeny or potential adaptations of behaviours in different animal systems. Studies on collective behaviour have yet more challenges to overcome due to increased dimensionality in the system. Even though the endeavors have been facing difficulties in precisely quantifying and representing the complexity of the collectives, recent developments in technologies have advanced the field greatly. With the advanced tracking and imaging technologies and theoretical tools on evolution, studying animal collective behaviour from an evolutionary perspective is becoming more tractable. In an attempt to contribute to such efforts, my thesis focused on investigating the evolutionary explanations of the natural variation in aggregation behaviour across the wild populations of C. elegans nematodes, a famous model organism in the field of biology. This species has a rich database and resources on natural diversity and genomic information as well as a well-characterised behaviour repertoires. With abundant resources and conceptual knowledge readily available to this species, I asked if the aggregation behaviour in this species naturally diverged in the wild populations, and if the variation pattern could suggest a potential adaptation to different environments via natural genetic variations. Chapter 1 has investigated this possibility in a small selected set of genetically divergent strains isolated from various natural habitats of the globe. Aggregation behaviour assay was conducted on this set of strains, and sensitive measures that can quantify the natural variation and the dynamics of the behaviour were developed. High levels of variation were revealed in the aggregation traits among the strains, and moreover, the behavioural variation was found to be correlated with environmental categories and genetically inheritable. This suggested that aggregation behaviour in C. elegans could have diverged in the wild, and supported in expanding the results to broader global samples in Chapter 3. Chapter 2 has developed from the result of Chapter 1, and focused on the potential connection between aggregation and individual foraging behaviour in C. elegans. Since the environmental categories of Chapter 1 were postulated to affect the foraging behaviour of C. elegans, high levels of association was speculated between these collective and individual behaviours. Individual foraging assays using the same divergent set of strains were 4 conducted and foraging-related locomotive features were quantified. Using the Gaussian Hidden Markov Model, the dwelling probabilities of different strains were estimated, and it was revealed that the variation pattern of individual dwelling explains a big portion of the natural variation in collective aggregation behaviour. This led to a possibility that aggregation in C. elegans could be a self-organised foraging behaviour, and allowed the conceptual decomposition of aggregation into three organisational levels of collective, inter-individual, and individual components. Chapter 3 culminates with the expanded analyses onto 185 global wild strains, investigating the associations between the natural variation in aggregation behavioural components and the specific environmental and genetic correlates. Generalised Least Squares model revealed environmental associations to elevation and possibly to temperature fluctuations. Genome Wide Association analyses found correlations to genetic loci involved in the neuronal processes and foraging modulations in C. elegans. These results support the conjectures that natural variation in C. elegans aggregation behaviour may reflect potential divergence in animal’s adaptation in foraging behaviour and oxygen preferences. With caveats and limitations in mind, I was able to not only quantitatively measure C. elegans aggregation with precision in the laboratory, but also revealed its various associative genetic and environmental factors. Through this project I hope to provide a study system for collective behaviour and contribute to our understanding of evolution of animal collective behaviour.