Diet related adaptations across a small mammal hybrid zone

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Nielsen, Danny

Issue Date

2022

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Dissertation

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desert , diet adaptations , hybridization , microbiome , small mammals , woodrats

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Hybrid zones have long been used to investigate divergence and speciation. Many hybrid zones occur across sharp ecotones—areas characterized by transition in biological community composition. Such hybrid zones are often the result of secondary contact—when populations that descended from a common ancestral population come into contact after a period of allopatry. These populations may have accumulated differences via neutral process (i.e., genetic drift) or adaptation to differing environments. In the absence of complete reproductive isolation, genes may then flow between these differentially adapted populations. Vegetation turnover is common across ecotones, and plant availability is important to mammalian herbivores that consume plants that often produce toxic plant secondary compounds (PSCs). Availability of diet plants for which mammalian herbivores are adapted may limit movement and underlie pre- and post-zygotic isolating mechanisms across sharp ecotones. I studied diet and diet-related adaptions in a mammalian hybrid zone between two species of woodrat (Neotoma) that occurs across a sharp ecotone characterized by differences in plant community composition. Using live-trapping and field-based experiments, coupled with amplicon sequencing of DNA extracted from woodrat feces, I quantified variation in diet, diet preference, and gut microbiome composition between N. lepida (desert woodrat) and N. bryanti (Bryant’s woodrat), and F1 and backcross hybrids. I found that each parental species maintains distinct diets that contain plants that produce toxic PSCs but these plants were also among the most nutritional across the site. Furthermore, these dietary differences were maintained across seasons and years that spanned more wet to more dry periods. These diets were also associated with differences in microbiome composition, and while diet was primarily predicted by habitat, microbiome composition was constrained by genotype. I then used laboratory-based feeding experiments to determine how each species responds—physiologically, genetically, and behaviorally—to their native and non-native diet. Diet experiments were followed with 16S rRNA sequencing of contents from woodrat caecum, as well as RNA sequencing of tissue from the liver and caecum of woodrats. Response to diet treatments was asymmetrical, with N. lepida exhibiting greater response behaviorally, genetically, and in gut microbiome composition. Gene expression in liver was strongly influenced by species and exhibited little effect of diet treatment, but differential expression of genes in the caecum exhibited strong species by diet interaction effects. Neotoma lepida exhibited a strong diet effect in genes expressed in the caecum, as well as in differences in microbiota of the caecum. These results suggest that interactions between host genes and microbes contained in the caecum may play a role in the metabolism of plant PSCs. These field-based observations and laboratory-based experiments add to our understanding of how diet and diet-related adaptations may influence gene flow across this small mammal hybrid zone.

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