Graduation Year

2026

Document Type

Dissertation

Degree

Ph.D.

Degree Name

Doctor of Philosophy (Ph.D.)

Degree Granting Department

Public Health

Major Professor

Lynn B. Martin, Ph.D.

Committee Member

Derek Wildman, Ph.D.

Committee Member

Chengqi Wang, Ph.D.

Committee Member

Diego Santiago Alarcon, Ph.D.

Keywords

Enteric Pathogens, Gene Co-Expression Networks, Innate Immunity, Passer domesticus

Abstract

Biological invasions offer natural experiments for studying how organisms cope with ecological novelty. Although invasion success is often attributed to enemy release, introduced organisms do not enter enemy-free environments. Instead, they enter heterogeneous landscapes in which some familiar enemies are absent, others remain, and entirely novel enemies may be encountered. The question, then, is how invaders (hereafter non-natives) are poised to respond to these threats? This dissertation examines whether successful invasions in house sparrows (Passer domesticus) is associated with shifts in pathogen exposure, immune dynamics in blood, gut physiology, and gene co-expression network structure.

Chapter 1 is at the population/ecological scale and tests whether the Enemy Release Hypothesis applies to enteric pathogens. Sampling 200 sparrows across eight populations across the world, I quantified the prevalence of avian pathogenic Escherichia coli (APEC) and Salmonella enterica. S. enterica infections were rare across all populations. APEC prevalence, however, depended on the interaction between population status (native vs non-native) and local urbanization. In highly urban environments, non-native sparrows showed lower APEC prevalence than natives, consistent with enemy release; however, in less urban areas, the relationship reversed. Together, these results challenge the generality of the ERH and suggest that pathogen pressure on invaders is jointly shaped by environmental context, consistent with a geographic mosaic of host–pathogen interactions.

While Chapter 1 asks about differences in pathogen prevalence, Chapter 2 asks how native and non-native respond to the same standardized immune challenge. Specifically, I asked whether constitutive toll-like receptor expression (TLR-2 and TLR-4) and cytokine responsiveness (IL-1β and IL-10) are decoupled in non-native sparrows in a manner consistent with balancing the risk of immunopathologies against the risk of direct damage. Following an LPS challenge, non-native sparrows showed an inverse relationship between baseline TLR-4 expression and the magnitude of the IL-1β and IL-10 response. Sparrows with higher surveillance showed a smaller cytokine response, while birds with lower surveillance showed a larger one. Body condition predicted cytokine responsiveness similarly in both groups. Altogether, non-native sparrows have decoupled surveillance from inflammatory response in a way that natives have not, with a strategy that maintains pathogen vigilance without possibly paying the full costs of a robust inflammatory reaction.

Next, I moved to looking at physiology in the tissue most exposed to novelty: the gastrointestinal tract. Chapter 3 examines whether and how the gut transcriptome differs between native and non-native sparrows. Using mRNA-seq on duodenal tissue from 24 adult males across four native and four non-native populations, I identified 510 differentially expressed genes, with 199 upregulated and 311 downregulated in non-natives. Functional enrichment revealed that non-natives upregulated processes tied to DNA replication, DNA repair, and epithelial barrier function. This pattern points to a structural mode of defense in which non-native sparrows maintain gut integrity through epithelial maintenance and molecular repair, rather than through heightened immune activation. Such a strategy may help preserve gut function in unfamiliar microbial environments while reducing the energetic and immunopathological costs of immune activation, and is consistent with a tolerance-leaning physiology.

Chapter 4 moves from the composition of gene expression to its architecture, asking whether the structure of gene co-expression networks themselves differs between native and non-native populations. Using the same duodenal transcriptomes, I constructed weighted gene co-expression networks separately for each population type. Non-native sparrows exhibited substantially lower global connectivity yet higher structural modularity and reduced functional overlap among modules. In a combined network including all individuals, non-native-associated genes occupied peripheral, locally cohesive positions rather than central, globally integrated ones, a pattern consistent with regulatory change occurring where pleiotropic costs are lowest. Critically, neither climatic predictability nor genetic ancestry predicted network architecture; only population status did. To my knowledge, these results represent the first empirical evidence that vertebrate gene co-expression networks are restructured across populations differing in ecological context, and they suggest that network topology can serve as a biologically meaningful phenotype in its own right.

Together, these chapters reveal a strategy of nuanced regulation: some defenses are restrained where systemic activation would be costly and others are reinforced to protect against pathogen entry. The convergence of these signals across scales suggests that house sparrow invasion success is shaped less by the magnitude of defense than by how defense is organized. More broadly, this framework reframes the unit of biological inference from things to processes: treating network organization as a phenotype. If modularity confers resilience under unpredictable conditions, then the same properties that allow non-native populations to persist in novel environments may also predict how species cope with the rapid environmental shifts driven by urbanization, climate change, and the emergence of novel pathogens.

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