Global proliferation of the endosymbiont Wolbachia

Wolbachia bacteria are the most widespread symbionts on earth, infecting the cells of about half of all insects species, as well as other arthropods. Virus-blocking Wolbachia that naturally infect Drosophila melanogaster are used as a biocontrol in mosquito-vector populations to limit the transmission of deadly viruses like dengue and Zika. My research takes an integrative approach to understand how interactions between Wolbachia, their host species, and the environment mediate the spread and maintenance of Wolbachia infections in insects.

Wolbachia maternal transmission and polymorphism

Maternal transmission is key to the maintenance of Wolbachia infections in host populations. I am interested in how imperfect Wolbachia transmission (maternal leakage) contributes to infection frequency fluctuations in nature. The frequency of wYak Wolbachia varies with altitude in populations of D. yakuba on the island of São Tomé off West Africa. We recently found that wYak transmission is particularly leaky at high altitude on the island, where conditions are relatively cool and humid. In the lab, cool temperatures reduce wYak titer and increase maternal leakage to levels observed on São Tomé. Our modeling suggests that altitudinal variation in wYak frequencies on São Tomé can be explained by temporal variation in rates of maternal leakage or spatial variation in Wolbachia effects on host fitness and reproduction. Because maternal transmission is usually perfect in the lab (unlike in nature), our results on wYak maternal leakage open the door to exciting new cellular analyses of Wolbachia transmission in the lab.

Wolbachia effects on host physiology and behavior

The initial spread of Wolbachia in host populations is driven by beneficial effects on host fitness. These host benefits are key to explaining the global proliferation of Wolbachia, yet we have a poor understanding of how Wolbachia alter components of host fitness in natural populations. To address this gap in knowledge, my research aims to improve our basic understanding how Wolbachia affect host physiology and behavior. Our recent project spearheaded by Chelsey Caldwell, a UM undergraduate student, found that Wolbachia have pervasive effects on host temperature preference. Insects rely on thermoregulatory behavior to maintain body temperature within a narrow range, so changes to temperature preference likely have important implications for host performance and fitness. Chelsey recently presented her findings at the 2020 UM Conference on Undergraduate Research!


Evolution at the interface of toxin binding in a predator-prey arms race

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​I am interested in how underlying patterns of genetic variation permit and/or constrain (co)adaptation among interacting species. My dissertation in the Brodie lab examined adaptation in the coevolutionary arms race between garter snakes and their toxic prey, Pacific newts. I explored how molecular evolution, gene flow, and historical biogeography impact adaptation at the interface of toxin binding.

Convergent evolution of a conserved protein

In western North America, two separate lineages of the common garter snake independently evolved resistance to tetrodotoxin (TTX), the deadly neurotoxin found in newts. I found that both lineages convergently evolved resistance through a common series of amino acid changes to the Nav1.4 skeletal muscle sodium channel that disrupt toxin binding. In each instance, evolution proceeded through the same first-step mutation to the pore of the channel, suggesting the initial change had permissive effects for subsequent increases in resistance.

Once TTX-resistant mutations accumulated in Nav1.4, we also found that negative trade-offs occur with sodium channel function and muscle performance. Our results indicate that costs develop as a consequence of accumulating mutations in the arms race that beneficially interfere with toxin binding. The evolutionary trajectory of Nav1.4 seems to strike a balance between TTX resistance and the maintenance of conserved channel function. Balancing selection and the pleiotropic effects of mutations to Nav1.4 likely contribute to variation in TTX resistance across western North America.

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Asymmetries in the arms race

Reciprocal adaptation is the hallmark of a coevolutionary relationship, but the symmetry of evolution in each species is often untested. We recently assessed whether snakes and newts exhibit symmetrical evidence of local co-adaptation in the classic example of a geographic mosaic of arms race coevolution. Levels of snake resistance and newt toxins are closely matched across the landscape, implying that mosaic variation in the armaments of both species is the result of local pressures in the arms race. By the same token, phenotypic and genetic variation in snake resistance deviates from neutral expectations of population genetic structure. Contrary to conventional wisdom, however, we found that landscape variation in newt toxins is best predicted by population genetic differentiation, as opposed to predator resistance. Newt populations seem to structure variation in toxin levels, which in turn influences local levels of resistance in garter snakes. Our results imply that neutral processes like gene flow—rather than reciprocal adaptation—may represent the greatest source of variation across the coevolutionary mosaic.

Patterns of genetic diversity in sympatric lizards

Genetic variation is a basic requirement for evolution and adaptation. Theory suggests that genetic diversity should increase with effective population size and the decreasing effects of drift. For my Master's research in the Routman lab, I tested how levels of genetic diversity vary in sympatric populations of lizard species in the Mojave Desert that differ in population size and other ecological factors. At both mitochondrial and nuclear loci, we found that abundant, short-lived species had significantly higher estimates of diversity than less abundant, long-lived lizards. High diversity values in the abundant species are likely due to a number of demographic factors, including larger effective population sizes, short generation time, and high rates of gene flow with surrounding populations.

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