Strong Bottlenecks Constrain Adaptive Coevolution in a Host–Parasite Metapopulation

Although parasites are well-known for adaptively evolving in order to exploit their hosts, they may experience strong genetic drift during transmission bottlenecks when infecting a new host. Host population structure and host population bottlenecks can also lead to genetic drift effects in parasite populations, constraining their adaptive evolution further. Here, we investigate the role of host population structure on the evolution of the microsporidian parasite Hamiltosporidium tvaerminnensis in a dynamic metapopulation of its microcrustacean host Daphnia magna. In following whole-genome allele frequencies of 59 host and parasite subpopulations for up to 10 years, we found that both antagonists showed patterns of co-dispersal and isolation-by-distance, but allele frequencies were much more dynamic in the host, where we found signatures of recurrent genetic bottlenecks. In the parasite, we observed high levels of shared heterozygosity among subpopulations but also subpopulation-specific runs of homozygosity (ROHs). We hypothesise that deleterious ROHs, which originate from loss of heterozygosity events during asexual recombination, are fixed in subpopulations following host-mediated parasite population bottlenecks when host and parasite co-disperse into a habitat patch where the parasite is not yet present. Thus, host population structure and metapopulation dynamics leave a clearly traceable genomic signature in the coevolving parasite. Contrary to the prevailing assumption that parasites evolve at higher rates than their hosts, our study not only suggests that parasites can evolve more slowly than their host, but also that host dynamics can accelerate drift processes in the parasite.