Coevolution occurs when species exert reciprocal natural selection on each other such that adaptation is interdependent. The process of coevolution can unfold diffusely within guilds of species, between species pairs, and between loci. It is hypothesized to have driven much of the diversification of life. Therefore, understanding the mechanistic basis of coevolution, from genes to phenotypes to fitness, is of central importance in biology.
The image above summarizes how much of the research in our lab is organized. We study how “keystone molecules“—those biomolecules that have outsized ecological impacts—drive coevolution between species. Our research often focuses on toxins produced by plants, animals, and microbes that are used in defense and offense. Since 2007, we have studied the evolution of herbivory and host plant specialization in the drosophilid fly Scaptomyza flava, an herbivore of mustards like the genetic model plant Arabidopsis thaliana. This fly species is phylogenetically nested in the paraphyletic Drosophila subgenus. This means that in essence, S. flava is a Drosophila that attacks Arabidopsis. We have identified some of the molecular mechanisms this fly uses to cut into hosts (the plant-penetrating ovipositior), how it lost yeast-sensing odorant receptors and gained other odorant receptors that detect volatile mustard oils and allows them to find host plants, how it detoxifies mustard oils, and how its interactions with bacteria influence its life history. We have also taken a genome’s eye point of view to determine if patterns of chemosensory and detoxification gene family evolution can be predicted from understanding the life history transition to herbivory from non-herbivorous ancestors. We are using this system to study how fly populations adapt to different host plant species in single host plant and mixed host plant environments (mosaics of hosts) and how functional genetic variation can be maintained by spatially varying natural selection through such heterogeneous environments (the so-called Levene Model).
We often rely on genome editing and engineering to study the molecular mechanisms of chemical co-evolution between species. Three case studies illustrate how. The first case traced the origins of cardiac glycoside resistance in monarch butterflies, which sequester these toxins in defense against birds, and how some monarch-eating birds evolved to resist those toxins too. The second case focused on distinct waves of neurotoxic terpenoid diversification in plants over the past 400 million years, along with co-diversification of herbivorous insects and their predators that evolved resistant GABA receptors. The third case illuminated how apoptotic toxin-encoding genes in bacteria were captured by drosophilids and many other insect species through horizontal gene transfer, became integrated into the fly innate immune system, and are used as defensive weapons against parasitoid wasps.
This latter strand is becoming a major focus of the lab as we seek to understand how animals evolved innate immune mechanisms against other animals, particularly in light of the risks of auto-immunity. This is an important question given that macroparasites are more important than microparasites in shaping recent local adaptation in humans and that over 2 billion people (one quarter of all people) are infected with macroparasites right now on the planet. The fly-wasp model is useful given the powerful tools that allow us to manipulate it genetically and because the immature stages of the wasps feed on the hemolymph (invertebrate blood) much like blood-feeding nematodes like hookworms and whipworms and flukes (aka schistosomes). Our bodies have evolved the capacity to resist these macroparasites to a degree but we still do not have a good understanding of how. This is important if we are to better understand exactly how “Type 2” immunity is triggered.
We also study signal-receiver coevolution that hinges on single molecules like the opsins that allow hummingbirds to see the nectar plants that have evolved to exploit their visual systems. Our research on Broad-tailed hummingbirds and their nectar plants focuses on this question and the genome-wide architecture associated with foraging traits like bill size and shape and arrival time at the breeding grounds. This research dovetails with Noah’s long-standing interest in coevolution between birds and other species, like Galapagos birds and their parasites, which he studied for his dissertation research. Finally, coevolution between the sexes of the same species is also being pursued by two postdocs in the lab, in trees on the one hand and butterflies on the other.
Finally, through a new grant from the Simons Foundation, with colleagues at Berkeley and the Smithsonian Tropical Research Institute in Panama, we are studying how biotic interactions shape the evolution and diversity of the most diverse ecosystems on the planet: tropical forests. Stay tuned for more on this project.
More than anything else, the particular research interests of each lab member help determine our lab’s trajectory.
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