Functional immunogenetic variation, rather than local adaptation, predicts ectoparasite infection intensity in a model fish species.

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.

Expansion of frozen hybrids in the guppy ectoparasite, Gyrodactylus turnbulli.

Hybridization is one of the major factors contributing to the emergence of highly successful parasites. Hybrid vigour can play an important role in this process, but subsequent rounds of recombination in the hybrid population may dilute its effects. Increased fitness of hybrids can, however, be frozen by asexual reproduction. Here, we identify invasion of a 'frozen hybrid' genotype in natural populations of Gyrodactylus turnbulli, a facultatively sexual ectoparasitic flatworm that causes significant damage to its fish host. We resequenced genomes of these parasites infecting guppies from six Trinidad and Tobago populations, and found surprisingly high discrepancy in genome-wide nucleotide diversity between islands. The elevated heterozygosity on Tobago is maintained by predominantly clonal reproduction of hybrids formed from two diverged genomes. Hybridization has been followed by spread of the hybrids across the island, implying a selective advantage compared with native genotypes. Our results thus highlight that a single outcrossing event may be independently sufficient to cause pathogen expansion.

Gene duplications, divergence and recombination shape adaptive evolution of the fish ectoparasite Gyrodactylus bullatarudis.

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.

Immunogenetic novelty confers a selective advantage in host-pathogen coevolution.

The major histocompatibility complex (MHC) is crucial to the adaptive immune response of vertebrates and is among the most polymorphic gene families known. Its high diversity is usually attributed to selection imposed by fast-evolving pathogens. Pathogens are thought to evolve to escape recognition by common immune alleles, and, hence, novel MHC alleles, introduced through mutation, recombination, or gene flow, are predicted to give hosts superior resistance. Although this theoretical prediction underpins host-pathogen "Red Queen" coevolution, it has not been demonstrated in the context of natural MHC diversity. Here, we experimentally tested whether novel MHC variants (both alleles and functional "supertypes") increased resistance of guppies (Poecilia reticulata) to a common ectoparasite (Gyrodactylus turnbulli). We used exposure-controlled infection trials with wild-sourced parasites, and Gyrodactylus-naïve host fish that were F2 descendants of crossed wild populations. Hosts carrying MHC variants (alleles or supertypes) that were new to a given parasite population experienced a 35-37% reduction in infection intensity, but the number of MHC variants carried by an individual, analogous to heterozygosity in single-locus systems, was not a significant predictor. Our results provide direct evidence of novel MHC variant advantage, confirming a fundamental mechanism underpinning the exceptional polymorphism of this gene family and highlighting the role of immunogenetic novelty in host-pathogen coevolution.