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Title: Host speciation and microbiomes: ecological and evolutionary factors shaping gut microbial communities in Darwin's finches
Abstract: The bacterial communities associated with host organisms, or microbiomes, are an integral aspect of host health, development, and evolution. Characterization of microbiomes in wild animals are essential to our understanding of co-evolutionary histories among animal lineages. However, it is difficult to disentangle the numerous variables that can affect the composition of this bacterial community. Therefore, I investigated the factors that potentially shape gut microbiomes in one of the best studied avian lineages in the world, Darwin’s finches in the Galápagos Archipelago. The distribution of species across the islands allowed for independent sampling in ecologically distinct habitats. Given their well-characterized evolutionary history, Darwin’s finch species provided an ideal study system for testing the effect of co-phylogeny on the gut microbiome in the context of ecological factors.
First, I comprehensively sampled nine Darwin’s finch species on Santa Cruz Island, spanning the extremes of the ecological habitats. The microbial diversity was characterized using 16S rRNA sequencing. In addition to microbiome data, host phylogeny, stable isotope analysis, and first foraging observations in the field were used to place the microbiome characterization in their evolutionary and ecological context. Applying a variety of methods to examine the relationship between the gut microbiome and these factors, I detected a clear effect of habitat and correlation of the microbiome with both host phylogeny and dietary preferences, with foraging data uniquely explaining portions of the variation seen in the gut microbiome.
Next, the recent introgression from the medium tree finch (Camarhynchus pauper) into the small tree finch (C. parvulus) on Floreana Island was used as a case study for the effect of species identity and genetic background on the gut microbiome. Due to the morphological similarity between small and hybrid tree finches, I genotyped and morphologically characterized all tree finches in combination with analyzing their microbiomes. Though overall patterns in beta diversity were similar across genetic clusters, differential abundance analysis with both 16S and metagenomic data demonstrated that the gut microbiomes of hybrid tree finches are more similar to those of their paternal species, the small tree finch.
Finally, I interrogated the remaining ground finch species from Floreana Island as an independent sample for signatures of co-diversification and performed a meta-analysis with the overlapping species between the two islands. Darwin’s finch gut microbiome samples were consistently different between the highland and lowland habitats on each island. Additionally, they were significantly different between the highland habitats of the two islands, but not the lowland habitats, signifying a clear environmental effect independent of host species, likely as a result of more divergent flora present in the highlands than the lowlands.
Altogether, this dissertation provides three separate but interconnected lines of evidence that are consistent with a model of microbiome assembly in which environmental filtering via diet and habitat are primary determinants of the bacterial taxa present with secondary influence from the evolutionary history between hosts. These studies demonstrate the necessity of comprehensive metadata for the correct interpretation of patterns observed in host-associated bacterial communities and provide foundational knowledge for future work in understanding the complex dynamics of microbiome assembly.
Committee: Colleen Cavanaugh (Advisor), Eric Alm, Scott Edwards, Peter Girguis