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  1. Abstract

    Reciprocal co‐evolving interactions between hosts and parasites are a primary source of strong selection that can promote rapid and often population‐ or genotype‐specific evolutionary change. These host–parasite interactions are also a major source of disease. Despite their importance, very little is known about the genomic basis of co‐evolving host–parasite interactions in natural populations, especially in animals. Here, we use gene expression and sequence evolution approaches to take critical steps towards characterizing the genomic basis of interactions between the freshwater snailPotamopyrgus antipodarumand its co‐evolving sterilizing trematode parasite,Microphallussp., a textbook example of natural coevolution. We found thatMicrophallus‐infectedP. antipodarumexhibit systematic downregulation of genes relative to uninfectedP. antipodarum. The specific genes involved in parasite response differ markedly across lakes, consistent with a scenario where population‐level co‐evolution is leading to population‐specific host–parasite interactions and evolutionary trajectories. We also used anFST‐based approach to identify a set of loci that represent promising candidates for targets of parasite‐mediated selection across lakes as well as within each lake population. These results constitute the first genomic evidence for population‐specific responses to co‐evolving infection in theP. antipodarum‐Microphallusinteraction and provide new insights into the genomic basis of co‐evolutionary interactions in nature.

     
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