Genomics of Host-Parasite Coevolution: A Test of Arms Race and Red Queen Dynamics in a Wild Insect System

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Parasites and their hosts evolve together. Our research will test hypotheses about the genomic basis of this mutually-dependent coevolution using a high-profile, wild insect system undergoing extremely rapid evolution: field crickets that are fatally attacked by an eavesdropping endoparasitoid fly, Ormia ochracea.Coevolution occurs when defensive adaptations of a host species drive the evolution of counter-adaptation in their natural enemies, which in turn exerts selection favouring host adaptation. Theory predicts that this back-and-forth can occur via two general modes: in arms race (AR) coevolution, new host and parasite adaptations and counteradaptations evolve via selective sweeps. This model predicts that host and parasitoid genomes should show signatures of positive selection and recurrent selective sweeps. In contrast, Red Queen (RQ) models predict an ongoing tug-of-war which neither host nor parasite ever "wins". This model predicts that host adaptations and parasite counteradaptations should be maintained in a polymorphic state by balancing selection. We will take advantage of the clear predictions about genomic selection that these models make to test them in the cricket/fly system, a textbook exemplar for rapid adaptive evolution in nature. We will use a population genomics approach with cutting-edge whole genome resequencing data to test a series of hypotheses that will reveal whether one, the other, or both modes of coevolution explain coevolutionary adaptation in this system, what genomic 'hotspots' are involved, and insight into their function. We will examine this in two contexts. Our project focuses on fly and cricket populations in Hawaii and North America. Fly larvae fatally consume hosts, exerting well-studied selection on the crickets: in Hawaii, males repeatedly evolved song-loss adaptations that erase sound-producing wing structures, protecting them from flies. These host adaptations exert pressure on the flies to find silent crickets using other sensory modalities. In contrast, North American flies attack different host species which have not evolved male-silencing adaptations, yet have different male advertisement songs to which the flies are locally adapted. This set-up provides an unparalleled opportunity to test classic coevolutionary models underlying fly counter-adaptation to host defences (Hawaii) and fly local adaptation to host signal variation (North America). Our project will gauge evidence for AR and RQ in driving parasite counter-adaptations to host defenses, allowing that both might operate simultaneously. We will provide further advances by partitioning AR and RQ dynamics across the fly genome and relate them to functional information, and we will examine shared genetic bases of coevolution when a parasite is limited to one host species versus adaptation to multiple host species. A major benefit is our plan to examine coevolutionary dynamics of traits beyond immunological adaptations, which have historically been a focus of genetic approaches, and our research will also provide cutting-edge genomics resources for an insect model used in applied, bio-inspired research on nanotechnology of acoustic reception and hearing.