The ecology and fitness consequences of gut microbiome variation in Sable Island feral horses (Equus caballus)

Abstract
Gut microbiomes are understood to be integral to the ecology and evolution of animal life, but until very recently, the scientific literature has lacked robust empirical characterization of the host genetic basis and fitness consequences of microbiome variation within wild animal populations. As a closed population of free-living but exhaustively surveyed fate-known individuals which are obligately reliant on their gut microbiomes, the feral horses of Sable Island (Nova Scotia) provide a tractable study system in which to study the ecology, host-to-host transmission, and fitness consequences of microbiome variation in the wild. In this thesis, I begin by characterizing the ecological determinants of the Sable Island horse hindgut microbiome (Chapter 2) and validate the use of shallow shotgun metagenomic sequencing methods for characterizing diverse microbial communities in the horse hindgut (Chapter 3). In applying a shallow shotgun metagenomic sequencing method to a dataset of 2394 fecal samples from 794 individuals spanning 7 years of collection, I find evidence that variation the gut microbiome is visible to host-level selection (Chapter 4). Further quantitative genetic analyses of these data reveal that microbiome features are weakly heritable on average (Chapter 5), suggesting a limited capacity for the microbiome to rapidly respond to selection; but animal model and eco-phylogenetic null model results independently provide evidence that the social dispersal of microbes between horses is an important determinant of microbiome structure. Furthermore, the microbiota which show the strongest evidence for social structuring are those which are most consequential for horse survival. These findings support hypotheses that non-genetic inheritance mechanisms (microbe dispersal) could critically underlie the ability for microbiomes to adaptively respond to selection on ecologically-relevant timescales. However, host inbreeding may constrain the capacity for microbiome variation to adaptively respond to host-level selection, since microbe responses to inbreeding were negatively associated with the estimated effects of those same microbiota on horse survival (Chapter 6). The proximate environmental and host genetic mechanisms underpinning microbiome variation, patterns of context-specific selection, and strain-level transmission remain to be characterized in detail. Nonetheless, this thesis contains tentative but important empirical milestones in describing the eco-evolutionary significance of host-associated microbiomes in the wild.
Description
Keywords
holobiont, metagenomic, non-genetic inheritance, quantitative genetics, symbiosis, wildlife
Citation
Stothart, M. R. (2023). The ecology and fitness consequences of gut microbiome variation in Sable Island feral horses (Equus caballus) (Doctoral thesis, University of Calgary, Calgary, Canada). Retrieved from https://prism.ucalgary.ca.