Ecology and evolution in microbial food webs

Abstract

All natural evolution occurs within an ecological context. Studying evolution in its simplest terms, for example via the LTEE, distills patterns and basic mechanisms. Yet biology is as much about complexity as it is about simplicity, and considering the factors that disrupt the patterns and complexify the mechanisms can reveal emergent truths. Microbial interactions are often studied as pairwise modules, yet they are influenced by the complexity of interaction networks. The prey in predator-prey interactions have competitors and cross-feeders, and the predators have their own predators and competitors to avoid or fight. In this thesis, I explore how behavior and evolution respond in multi-species microbial communities that are structured by predator-prey interactions. I focus on the bacterium Myxococcus xanthus, a social soil bacterium that swarms cooperatively through soil habitats, preying on other bacteria and fungi it encounters and, when nutrients are depleted, aggregating and developing into spore-filled fruiting bodies. The mechanisms, evolution, and origin of M. xanthus’s charismatic social traits offer a fascinating and fruitful target for this lens, and I investigate how M. xanthus responds over ecological and evolutionary time to interactions with lower trophic levels (prey) and higher trophic levels (predators). First, I construct a four-member community with two prey bacteria and M. xanthus and the bacterivorous nematode Caenorhabditis elegans as competing predators, and I measure the behavioral responses of the predators to each other. C. elegans generally avoids M. xanthus, leaving agar plates where it is the only food source (although worms who remain preferentially interact with M. xanthus over sterile buffer) and choosing patches of the lower-quality prey when M. xanthus is present in the patch of higher-quality prey. M. xanthus also shows a behavioral response to C. elegans, although this depends on third-party interactions – when the prey is of high quality, M. xanthus swarms faster in the presence of C. elegans. Next, I construct a three-member community comprising a food chain: Escherichia coli as a prey, M. xanthus as a mesopredator, and another bacterivorous nematode, Pristionchus pacificus, as an apex predator. I allow M. xanthus to evolve for 20 weeks in different community compositions: alone, with just E. coli, with just P. pacificus, or with both E. coli and P. pacificus. I first consider specific adaptation of evolved M. xanthus lineages to the different evolution treatments. Almost all lineages show evidence of adaptation to their own evolution environment, and it seems that exposure to at least one other organism during evolution provides some kind of benefit when encountering the other. However, exposure to both organisms is needed to do well in the three-member community. Swarming rates decreased relative to the ancestor, indicating that motility evolved across environments. I next consider trait-based evolution of M. xanthus in each of the communities in order to identify their contribution to the different long-term forces that shape M. xanthus as an organism. E. coli seems to simply offer a nutrient source, relaxing selection on starvation-related traits and allowing lack of maintenance to introduce phenotypic changes – in many cases, lineages that evolved in the presence of E. coli show lower levels of sporulation and no longer make fruiting bodies under starvation conditions. P. pacificus, on the other hand, selects for M. xanthus populations to form more and smaller fruiting bodies (although with unchanged levels of spore production), which may reflect an increased need for sheltering benefits. Strikingly, evolved lineages which descend from a variant of the wild type which contains a single point mutation in rpoB, and is therefore resistant to rifampicin, show a much smaller degree of trait-based evolution than lineages which descend from the wild type itself. This suggest that trade-offs between antibiotic resistance and anti-predator defense may shape evolutionary responses to inter-species antagonism under natural conditions. Finally, I argue for the development of microbial systems, such as the one I present here, both as a way to enrich the ecological, evolutionary, and mechanistic understanding of microbial communities and the specific trophic relationships which structure them and as a tool for addressing open questions about the evolution of predator behaviors and prey defenses more broadly. As we study interactions between simple ecological and evolutionary rules, surprising and beautiful complexity emerges.