Contrasting patterns of trematode and host snail dispersal across clusters of tropical crater lakes

Abstract

Abstract Background Comparing the genetic diversity and population structure of parasites and their hosts can improve understanding of their respective methods of dispersal, demographic histories, and factors driving genetic differentiation. In parasite taxa such as trematodes which have both intermediate and final hosts, comparative population-level analyses may also inform how each host influences gene flow among parasite populations. Here we aimed to assess how intermediate and final hosts influence trematode dispersal by examining the population genetic structure of the aquatic snail Bulinus tropicus and three trematodes that use it as intermediate host. Methods We used high-throughput amplicon sequencing to simultaneously genotype populations of B. tropicus in two clusters of crater lakes in western Uganda (823 snails, 15 lakes) and three infecting trematode taxa ( Petasiger sp., Echinoparyphium sp. and Plagiorchioidea sp.). For each taxon, we quantified genetic diversity in three mitochondrial markers and used analyses of molecular variance to test whether populations were genetically differentiated. Results Populations of B. tropicus were strongly genetically differentiated among individual crater lakes and lake clusters (Φ ST = 0.78), indicating limited inter-lake dispersal. Petasiger sp. haplotype diversity was on average twice as high as that of its intermediate snail host and did not display genetic structuring among lakes (Φ ST = 0.01). This parasite can therefore overcome the dispersal barriers encountered by its snail host, likely facilitated by mobile avian hosts, resulting in a single ‘panmictic’ region-wide population. Contrastingly, Echinoparyphium trematodes displayed less genetic diversity and significant genetic differentiation among lakes (Φ ST = 0.35), likely due to limited final host mobility. Finally, Plagiorchioidea sp. was restricted to five neighbouring lakes, and a single haplotype was identified in the 217 infected snails analysed, implying recent introduction into the crater lakes. Conclusions Contrasting patterns of genetic diversity and population structure among three parasitic trematodes and their common intermediate snail host illustrate how multi-host life cycles mediate dispersal dynamics and generate distinct evolutionary outcomes in hydrographically fragmented aquatic habitats. These findings demonstrate how multi-host life cycles shape parasite connectivity and evolution, and show that comparative population genetics can provide valuable insights into the dispersal ecology of understudied parasite species.