The cost of travel: How dispersal ability limits local adaptation in host–parasite interactions

Abstract

Classical theory suggests that parasites will exhibit higher fitness in sympatric relative to allopatric host populations (local adaptation). However, evidence for local adaptation in natural host–parasite systems is often equivocal, emphasizing the need for infection experiments conducted over realistic geographic scales and comparisons among species with varied life history traits. Here, we used infection experiments to test how two trematode (flatworm) species (Paralechriorchis syntomentera and Ribeiroia ondatrae) with differing dispersal abilities varied in the strength of local adaptation to their amphibian hosts. Both parasites have complex life cycles involving sequential transmission among aquatic snails, larval amphibians and vertebrate definitive hosts that control dispersal across the landscape. By experimentally pairing 26 host‐by‐parasite population infection combinations from across the western USA with analyses of host and parasite spatial genetic structure, we found that increasing geographic distance—and corresponding increases in host population genetic distance—reduced infection success for P. syntomentera, which is dispersed by snake definitive hosts. For the avian‐dispersed R. ondatrae, in contrast, the geographic distance between the parasite and host populations had no influence on infection success. Differences in local adaptation corresponded to parasite genetic structure; although populations of P. syntomentera exhibited ~10% mtDNA sequence divergence, those of R. ondatrae were nearly identical (<0.5%), even across a 900 km range. Taken together, these results offer empirical evidence that high levels of dispersal can limit opportunities for parasites to adapt to local host populations.

Divergence in host–parasite interactions during the cane toad's invasion of Australia

“…Thus, the parasite has undergone >1000 generations in 85 years since arriving in Australia compared with <100 host generations. Such disparity in generation times is often invoked to explain parasite advantage in local adaptation (Gandon, 2002;Johnson et al, 2021). Unexpectedly, our measures of feeding performance were positively, rather than negatively, affected by parasite burden, either as a main effect or in interaction with population age difference.…”

Co-structure analysis and genetic associations reveal insights into pinworms (Trypanoxyuris) and primates (Alouatta palliata) microevolutionary dynamics

“…When parasites show higher evolutionary rates and higher gene flow than their hosts, they are expected to be locally adapted, performing better in sympatric or home hosts than in allopatric or away hosts [ 19 , 58 ]. If we translate this into genetic terms, we expect locally adapted parasites to be more infective to genetically similar hosts than to genetically different hosts (see [ 59 ]). Indeed, we found that more divergent hosts were less susceptible to be parasitized by different pinworms haplotypes, suggesting higher performance of the parasite (infectivity) in genetically similar hosts compared to differing ones.…”

Mitigating human impacts including climate change on proliferative kidney disease in salmonids of running waters

“…The amount of gene flow between populations is important for assessing the geographic scale on which local adaptations may develop (Johnson et al., 2020). Gene flow should be expected through migration of infected fish between rivers, through release of infected statoblasts and through dislocation of infected bryozoans (Abd‐Elfattah, Fontes, et al., 2014; Abd‐Elfattah, Kumar et al., 2014).…”