Novel genomic approaches to study antagonistic coevolution between hosts and parasites

Host-parasite coevolution is ubiquitous, shaping genetic and phenotypic diversity and the evolutionary trajectory of interacting species. With the advances of high throughput sequencing technologies applicable to model and non-model organisms alike, it is now feasible to study in greater detail (a) the genetic underpinnings of coevolution, (b) the speed and type of dynamics at coevolving loci, and (c) the genomic consequences of coevolution. This review focuses on three recently developed approaches that leverage information from host and parasite full genome data simultaneously to pinpoint coevolving loci and draw inference on the coevolutionary history. First, co-genome-wide association study (co-GWAS) methods allow pinpointing the loci underlying host-parasite interactions. These methods focus on detecting associations between genetic variants and the outcome of experimental infection tests or on correlations between genomes of naturally infected hosts and their infecting parasites. Second, extensions to population genomics methods can detect genes under coevolution and infer the coevolutionary history, such as fitness costs. Third, correlations between host and parasite population size in time are indicative of coevolution, and polymorphism levels across independent spatially distributed populations of hosts and parasites can reveal coevolutionary loci and infer coevolutionary history. We describe the principles of these three approaches and discuss their advantages and limitations based on coevolutionary theory. We present recommendations for their application to various host (prokaryotes, fungi, plants, and animals) and parasite (viruses, bacteria, fungi, and macroparasites) species. We conclude by pointing out methodological and theoretical gaps to be filled to extract maximum information from full genome data and thereby to shed light on the molecular underpinnings of coevolution.