Author ORCID Identifier

https://orcid.org/0000-0002-4311-453X

Date Available

8-3-2024

Year of Publication

2024

Degree Name

Doctor of Philosophy (PhD)

Document Type

Doctoral Dissertation

College

Arts and Sciences

Department/School/Program

Biology

First Advisor

Dr. David W. Weisrock

Abstract

This dissertation bridges micro- and macroevolutionary approaches to understand the co-diversification of animal hosts and their gut microbiomes at different evolutionary timescales. I examined these dynamics using wild lemurs, a diverse Primate clade endemic to the island of Madagascar.

First, I tested the relative effects of host phylogenetic relationships, diet, and habitat in shaping the gut microbiome through deep evolutionary time and across distinct microbial kingdoms. I designed a natural experiment sampling feces from rainforest and dry forest lemur communities with similar phylogenetic assemblages and considerable variation in dietary strategy. Then, I amplified and sequenced two metabarcoding genes, the V4 region of the 16S rRNA gene and the V9 region of the 18S rRNA gene, to capture variation in prokaryotic and microeukaryotic communities, respectively. I found that more closely related species tended to share more similar gut prokaryomes. I also found that diet, but not habitat, contributed significantly to gut prokaryotic diversity, and that older prokaryotic clades had stronger associations with diet than younger ones. These findings suggest lemur hosts and gut prokaryomes co-diversified, but the subset of prokaryotes associated with diet were acquired in the common ancestor of major lemur clades and conserved through time as new species formed. Focusing on microeukaryotic diversity, I found no effect of host phylogeny, diet, or habitat. This may reflect a strong effect of the immune system in controlling the gut microeukaryome, as a greater proportion of microeukaryotes are pathogenic.

Then, I took a landscape metagenomic approach to elucidate patterns of co-diversification early in the speciation process. I examined evolutionary and microbiome dynamics in a purported hybrid species of brown lemur (Eulemur rufifrons x E. cinereiceps) endemic to southeastern Madagascar. I (1) tested a hypothesis of hybrid speciation using low-coverage genomes, (2) examined whether hybrid microbiomes were transgressive or intermediate relative to parental species, and (3) assessed whether gut microbiome divergence limited host gene flow. I generated genomic and microbiome (16S rRNA) data from feces I collected along a 180-km transect in the COFAV corridor. This region encompassed the entire purported hybrid zone, southeastern populations of E. rufifrons, and the majority of known E. cinereiceps populations. My results did not support a hypothesis of hybrid speciation, instead showing that hybridization was rampant throughout the study area, including isolated populations in distant forest fragments. Hybrid gut microbiomes were not distinguishable from parentals, and variation primarily arose due to geography. Furthermore, geography, not gut microbiome variation, explained patterns of gene flow. Therefore, I conclude that dispersal plays a dominant role in holobiont divergence when host reproductive barriers are incomplete.

By scaling from phylogenetic to population-level analyses, this dissertation illuminates the heterogeneous effects of host geography, diet, and evolution in shaping the gut microbiome (specifically, the prokaryome) along the speciation continuum. While geography and site-specific effects drive microbiome divergence in early stages of host evolutionary divergence, these effects are eventually overwhelmed by those of phylogenetic distance as species boundaries solidify. However, host diet constrains microbiome variation through deep evolutionary time. Finally, this research highlights the importance of conserving habitat corridors to maintain holobiont genetic diversity, and shows how microbiome co-divergence may have facilitated local adaptation in some of our closest living relatives.

Digital Object Identifier (DOI)

https://doi.org/10.13023/etd.2024.302

Funding Information

This dissertation was supported by NSF, Fulbright, HHMI Sustaining Excellence-2014 grant (#52008116), Society of Systematic Biologists Graduate Research Award, the University of Kentucky Ribble Endowment Fund, and a University of Kentucky Dean's Competitive Fellowship.

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