PhD defence: Veronica Sinotte
Title: The evolutionary ecology of social insect microbial symbioses
Associate Professor Jonathan Shik, https://www1.bio.ku.dk/english/research/ecology-evolution/groups/shik-group/ (chair)
Professor Tobi Kiers, Vrije Universiteit (https://tobykiers.com/)
Professor Stuart West, University of Oxford (https://www.zoo.ox.ac.uk/people/professor-stuart-west)
The social evolution of organisms and the microorganisms they interact with unequivocally shapes the complexity of life. Multicellular organisms evolved from social groups of related cells, and through this major evolutionary transition, interdependent, integrated, complex higher-level individuals such as animals were forged. Similarly, a subsequent transition occurred in cooperative social groups of related insects. The transition resulted in complex colonies known as superorganisms that can also be considered individuals from an evolutionary perspective. In superorganisms, insects are interdependent, dividing labour between reproductives and helpers, like the organismal germline and soma, and their actions are integrated to promote superorganismal reproduction.
These higher-level individuals, organisms and superorganisms, also interact with microbes such as bacteria and fungi, ranging from single species to complex communities of microorganisms. These microbes can be mutualistic, synergistically supporting host metabolism, defence, and development, or parasitic, harming host health and fitness. Consequently, hosts modify interactions with symbiotic microbes to promote beneficial associations, and overall, the interests of both hosts and microbes shape the evolution and ecology of symbioses.
This thesis explores symbioses between superorganismal social insects and their microbial partners. Among superorganismal clades, derived termites, bees, and certain ant species engage in ancient mutualisms with conserved and co-adapted microbes. First, I propose that natural selection at the level of the individual results in analogous mechanisms for microbiome management in superorganisms and multicellular organisms.
In Chapter 1, I hypothesize that superorganisms compartmentalize gut microbes across the division of labour to optimize the benefits of symbiosis, mirroring the distinct microbiomes found in different body regions of complex animals. I provide evidence from the literature in support of this hypothesis and outline predictions for compartmentalization based on characteristics of the major evolutionary transition.
In Chapter 2, I demonstrate extensive inheritance of the gut microbiome of fungus-farming termite colonies. Colonies ensure inheritance through a diverse microbial endowment carried by reproductives, who act as the superorganismal germ line that found new colonies and disseminate the co-evolved bacteria to their worker offspring. Next, I examine the impact symbionts have on hosts and the interplay between partners.
Chapter 3 follows the development of the gut microbiome in fungus-farming termites when they environmentally acquire their obligate fungal cultivar. The gut microbiome expands in both taxonomic and functional diversity after fungus acquisition, indicating that the bacterial microbiome is distinctively influenced by both the termites and the fungal cultivar. In Chapter 4, I demonstrate biased sex allocation in a population of termite colonies, which I posit may be caused by a bacterial reproductive parasite within the termites. Lastly, I contributed to two studies that emphasize the ecological importance of these superorganisms and their symbioses.
Chapter 5 highlights the impact of pesticides on key microbial symbionts and microbiome composition in honeybees. Chapter 6 then returns to the fungus-farming termites and reviews the collective role of termites and their microbial partners as ecosystem engineers. Overall, the thesis clarifies superorganismal symbioses within the framework of major evolutionary transitions, elaborates on interactions between complex hosts and symbiotic communities, and underlines the significance of these symbioses within ecosystems.