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Natural host populations differ in their susceptibility to infection by parasites, and these intrapopulation differences are still an incompletely understood component of host‐parasite dynamics. In this study, we used controlled infection experiments with wild‐caught guppies (Poecilia reticulata) and their ectoparasite Gyrodactylus turnbulli to investigate the roles of local adaptation and host genetic composition (immunogenetic and neutral) in explaining differences in susceptibility to infection. We found differences between our four study host populations that were consistent between two parasite source populations, with no indication of local adaptation by either host or parasite at two tested spatial scales. Greater values of host population genetic variability metrics broadly aligned with lower population mean infection intensity, with the best alignments associated with major histocompatibility complex (MHC) "supertypes". Controlling for intrapopulation differences and potential inbreeding variance, we found a significant negative relationship between individual‐level functional MHC variability and infection: fish carrying more MHC supertypes experienced infections of lower severity, with limited evidence for supertype‐specific effects. We conclude that population‐level differences in host infection susceptibility probably reflect variation in parasite selective pressure and/or host evolutionary potential, underpinned by functional immunogenetic variation. [ABSTRACT FROM AUTHOR]

Determining the molecular basis of parasite adaptation to its host is an important component in understanding host–parasite coevolution and the epidemiology of parasitic infections. Here, we investigate short‐ and long‐term adaptive evolution in the eukaryotic parasite Gyrodactylus bullatarudis infecting Caribbean guppies (Poecilia reticulata), by comparing the reference genome of Tobagonian G. bullatarudis with other Platyhelminthes, and by analysing resequenced samples from local Trinidadian populations. At the macroevolutionary timescale, we observed duplication of G‐protein and serine proteases genes, which are probably important in host–parasite arms races. Serine protease also showed strong evidence of ongoing, diversifying selection at the microevolutionary timescale. Furthermore, our analyses revealed that a hybridization event, involving two divergent genomes, followed by recombination has dramatically affected the genetic composition of Trinidadian populations. The recombinant genotypes invaded Trinidad and replaced local parasites in all populations. We localized more than 300 genes in regions fixed in local populations for variants of different origin, possibly due to diversifying selection pressure from local host populations. In addition, around 70 genes were localized in regions identified as heterozygous in some, but not all, individuals. This pattern is consistent with a very recent spread of recombinant parasites. Overall, our results are consistent with the idea that recombination between divergent genomes can result in particularly successful parasites. [ABSTRACT FROM AUTHOR]