Dispersal and drift drive diversity and structure in symbiont populations Restricted; Files Only
Chen, Jason (Spring 2024)
Published
Abstract
Many hosts are colonized by specific microbial symbionts which they rely on for proper development. Thus, host preference for optimally beneficial strains and competition between
strains are usually considered the predominant drivers of symbiont population structure. However, these cannot fully account for the high symbiont strain diversity and between-host heterogeneity observed in many symbioses. Understanding how symbioses assemble as ecological communities of microbes can provide insight into the population structure of symbionts.
The insect Anasa tristis relies on environmentally acquired bacterial symbionts (Caballeronia spp.) for normal growth and development. Although A. tristis imposes selection on environmental microbes to favor gut colonization by Caballeronia, how other drivers of community assembly contribute to Caballeronia community structure in this specialized host-
microbe symbiosis is unclear. In my dissertation, I demonstrate how dispersal and ecological drift contribute to naturally observed patterns of symbiont population structure.
First, I demonstrate that A. tristis nymphs are attracted to the feces of conspecific adults, which constitutes a behavioral adaptation for symbiont acquisition. Symbiont dispersal via fecal transmission results in strain-level specificity in symbiont acquisition, allowing for host-symbiont fidelity across generations without any apparent coevolutionary history or strain- specific functional differences for the insect host.
Next, I demonstrate that the composition of symbiont communities is determined by the order in which strains disperse into and colonize a host, or a priority effect. Within 24 hours, ingestion of one symbiont strain prevents superinfection by subsequently ingested strains. While colonization elicits tissue remodeling in the gut in a manner that prevents superinfection, this mechanism occurs too slowly to impose the priority effect on its own.
Finally, I demonstrate how ecological drift, in the form of transmission bottlenecks, maintains strain diversity and generates community heterogeneity. Drift generates heterogeneous colonization outcomes, mirroring those observed in nature, with inoculated strains segregating between different host individuals even when the strains are isogenic. Ecological drift also separates less competitive symbiont strains into different hosts than more competitive strains, even at high inoculation doses. Microscopy reveals that host anatomy also imposes single cell bottlenecks on isogenic bacteria as they colonize different gut crypts, resulting in within-host heterogeneity.
Table of Contents
Chapter 1. Introduction....................................................................................................................................... 1
Host-associated microbial communities and transmission mode......................................................................................................................... 1
Microbial community assembly......................................................................................................................... 2
Ecological Selection......................................................................................................................... 3
Diversification......................................................................................................................... 4
Dispersal......................................................................................................................... 5
Ecological Drift......................................................................................................................... 6
Model System......................................................................................................................... 8
Summary of Dissertation Chapters....................................................................................................................... 10
References....................................................................................................................... 11
Chapter 2. Specialized foraging behaviors maintain reliable environmental transmission in an insect-microbial mutualism................................................................................................................................. 16
Abstract....................................................................................................................... 16
Results and Discussion........................................................................................................................ 17
Methods....................................................................................................................... 32
Acknowledgments....................................................................................................................... 42
References....................................................................................................................... 43
Supporting Information....................................................................................................................... 52
Chapter 3. Strong priority effects without tissue remodeling in the assembly of an insect- microbe symbiosis................................................................................................................................. 54
Abstract....................................................................................................................... 54
Introduction....................................................................................................................... 55
Results....................................................................................................................... 57
Discussion....................................................................................................................... 68
Acknowledgements....................................................................................................................... 70
Methods......................................................................................................... 71
References...................................................................................................... 76
Supporting Information.................................................................................. 81
Chapter 4. Ecological drift during colonization drives within- and between-host
heterogeneity in animal-associated symbiont populations................................... 82
Abstract.......................................................................................................... 82
Introduction.................................................................................................... 83
Results............................................................................................................ 87
Discussion...................................................................................................... 96
Acknowledgements...................................................................................... 100
Methods....................................................................................................... 101
References.................................................................................................... 110
Supporting Information................................................................................ 120
Chapter 5. Conclusion........................................................................................... 131
Behavioral adaptions for symbiont acquisition and effects on symbiont community
structure....................................................................................................... 132
Colonization order governs the outcome of symbiont community assembly..................................................................................................................... 134
Transmission bottlenecks govern the outcome of symbiont community assembly....................................................................................................... 137
References.................................................................................................... 141
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