Coevolution at the Interface of Species Interactions
Michael TJ Hague
A cellular-genetic basis for endosymbiont prevalence
Endosymbioses are an intimate form of species interaction in which microbes reside within the cells of their host. These relationships influence basic aspects of host biology, evolution, and ecology. I study the spread and evolution of the most common endosymbionts in nature: maternally transmitted Wolbachia bacteria. Wolbachia infect about half of all insects species and biocontrol programs employ virus-blocking Wolbachia to prevent deadly human diseases in mosquito populations. My research program examines how cellular and genomic host-microbe interactions determine global Wolbachia prevalence and coevolution with hosts.
Transmission rates underlie Wolbachia prevalence
Wolbachia form facultative relationships with many insect species. My work and others' has shown that Wolbachia prevalence can vary widely among insect populations and environments, including in Australia. I recently made the exciting discovery that cold temperatures perturb the cellular basis of Wolbachia maternal transmission to host offspring, providing a simple explanation for latitudinal clines of Wolbachia prevalence. Decoupling temperate-evolved Wolbachia and host genomes further perturbs transmission in the cold, implying rapid co-adaptation to the climate in only the last ~5,000 years. This work points to temperature as a key determinant of global endosymbiont prevalence in insects and opens the door to many new research opportunities. Stay tuned!
Endosymbionts alter host fitness
Microbes have diverse effects on host physiology, behavior, and fitness. Wolbachia cells are found throughout many host tissues (e.g., the brain), yet we have a poor understanding of how somatic infections affect host fitness. Using a comparative approach, I've found that Wolbachia have pervasive effects on basic aspects of insect physiology and behavior. Thus far, my work has demonstrated how Wolbachia alter host activity levels and thermal preference. Chelsey Caldwell, a recent UM undergraduate student, spearheaded the project on host thermal preference and presented her findings virtually at the UM Conference on Undergraduate Research!
Evolution at the interface of toxin-binding in a predator-prey arms race
Intense reciprocal selection between natural enemies like predator and prey can lead to arms race coevolution. I study adaptation at the molecular interface of toxin-binding in the coevolutionary arms race between garter snakes and their deadly prey, Pacific newts. My dissertation examined how constraints on protein evolution, in conjunction with population structure, shape geographic variation in arms race dynamics across western North America.
Convergent evolution of a conserved protein
Arms race coevolution drives rapid adaptation and counter-adaptation, but functional trade-offs may also develop as a consequence. I found that multiple lineages of garter snakes independently evolved resistance to tetrodotoxin (TTX) via a repeated first-step mutation to the Nav1.4 skeletal muscle sodium channel that disrupts toxin-binding, implying that increases in resistance depend on an initial permissive mutation. In highly resistant snakes, accumulating mutations in the channel pore disrupt toxin-binding, but also generate negative trade-offs with Nav1.4 function and muscle performance. These results highlight how costs develop as beneficial mutations accumulate in the arms race. The evolutionary trajectory of Nav1.4 seems to strike a balance between increasing TTX resistance and maintaining the conserved function of the sodium channel. This pleiotropy associated with Nav1.4 evolution helps explain geographic variation in snake TTX resistance across western North America.
Asymmetries in the arms race
Reciprocal selection is the hallmark of a coevolutionary relationship, but the evolutionary response of each species may not be symmetrical. I tested whether snakes and newts have symmetrical evidence of co-adaptation across their range of sympatry. I found that levels of snake resistance and newt toxins are closely matched across the landscape, implying that geographic variation in both species' armaments is a result of the arms race. By the same token, phenotypic and genotypic variation in snake resistance exhibits a clear signature of local adaptation. Unexpectedly, however, landscape variation in newt toxins was best explained by the geographic structure of newt populations, not snake resistance. Newt populations seem to structure variation in prey toxins, which in turn influences local levels of resistance in predators. This surprising result suggests that neutral processes like gene flow—rather than reciprocal selection—represent the greatest source of variation across the geographic mosaic of coevolution.
Patterns of genetic diversity in sympatric lizards
Species differences in genetic diversity
Genetic variation is a fundamental requirement for evolution and adaptation. Genetic diversity should increase with effective population size and the decreasing effects of drift. For my Master's thesis, I tested how levels of genetic diversity vary in sympatric populations of lizard species in the Mojave Dessert 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. Higher diversity in the abundant species is likely due to a number of demographic factors, including larger effective population sizes, short generation times, and high rates of gene flow from surrounding populations.