An official website of the United States government
Summary In coevolving species, parasites locally adapt to host populations as hosts locally adapt to resist parasites. Parasites often outpace host local adaptation since they have rapid life cycles, but host diversity, the strength of selection, and external environmental influence can result in complex outcomes.To better understand local adaptation in host–parasite systems, we examined locally adapted switchgrass (Panicum virgatum), and its leaf rust pathogen (Puccinia novopanici) across a latitudinal range in North America. We grew switchgrass genotypes in 10 replicated multiyear common gardens, measuring rust severity from natural infection in a ‘host reciprocal transplant’ framework for testing local adaptation. We conducted genome‐wide association mapping to identify genetic loci associated with rust severity.Genetically differentiated rust populations were locally adapted to northern and southern switchgrass, despite host local adaptation to environmental conditions in the same regions. Rust resistance was polygenic, and distinct loci were associated with rust severity in the north and south. We narrowed a previously identified large‐effect quantitative trait locus for rust severity to a candidate YELLOW STRIPE‐LIKE gene and linked numerous other loci to defense‐related genes.Overall, our results suggest that both hosts and parasites can be simultaneously locally adapted, especially when parasites impose less selection than other environmental factors.
more »
« less
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 syntomenteraandRibeiroia 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 forP. syntomentera, which is dispersed by snake definitive hosts. For the avian‐dispersedR. 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 ofP. syntomenteraexhibited ~10% mtDNA sequence divergence, those ofR. ondatraewere 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.
more »
« less
- Award ID(s):
- 1754171
- PAR ID:
- 10447147
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Journal of Evolutionary Biology
- Volume:
- 34
- Issue:
- 3
- ISSN:
- 1010-061X
- Format(s):
- Medium: X Size: p. 512-524
- Size(s):
- p. 512-524
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract The location of parasites within individual hosts is often treated as a static trait, yet many parasite species can occur in multiple locations or organs within their hosts. Here, we apply distributional heat maps to study the within- and between-host infection patterns for four trematodes (Alaria marcianae, Cephalogonimus americanus, Echinostomaspp. andRibeiroia ondatrae) within the amphibian hostsPseudacris regillaand two species ofTaricha.We developed heatmaps from 71 individual hosts from six locations in California, which illustrate stark differences among parasites both in their primary locations within amphibian hosts as well as their degree of location specificity. While metacercariae (i.e., cysts) of two parasites (C. americanusandA. marcianae) were relative generalists in habitat selection and often occurred throughout the host, two others (R. ondatraeandEchinostomaspp.) were highly localised to a specific organ or organ system. Comparing parasite distributions among these parasite taxa highlighted locations of overlap showing potential areas of interactions, such as the mandibular inner dermis region, chest and throat inner dermis and the tail reabsorption outer epidermis. Additionally, the within-host distribution ofR. ondatraediffered between host species, with metacercariae aggregating in the anterior dermis areas of newts, compared with the posterior dermis area in frogs. The ability to measure fine-scale changes or alterations in parasite distributions has the potential to provide further insight about ecological questions concerning habitat preference, resource selection, host pathology and disease control.more » « less
-
Abstract Interactions between species are widely understood to have promoted the diversification of life on Earth, but how interactions spur the formation of new species remains unclear. Interacting species often become locally adapted to each other, but they may also be subject to shared dispersal limitations and environmental conditions. Moreover, theory predicts that different kinds of interactions have different effects on diversification. To better understand how species interactions promote diversification, we compiled population genetic studies of host plants and intimately associated herbivores, parasites, and mutualists. We used Bayesian multiple regressions and the BEDASSLE modeling framework to test whether host and associate population structures were correlated over and above the potentially confounding effects of geography and shared environmental variation. We found that associates' population structure often paralleled their hosts' population structure, and that this effect is robust to accounting for geographic distance and climate. Associate genetic structure was significantly explained by plant genetic structure somewhat more often in antagonistic interactions than in mutualistic ones. This aligns with a key prediction of coevolutionary theory that antagonistic interactions promote diversity through local adaptation of antagonists to hosts, while mutualistic interactions more often promote diversity via the effect of hosts' geographic distribution on mutualists' dispersal.more » « less
-
Complex life cycle parasites, including helminths, use intermediate hosts for development and definitive hosts for reproduction, with interactions between the two host types governed by food web structure. I study how a parasite's intermediate host range is controlled by the diet breadth of definitive host species and the cost of parasite generalism, a putative fitness cost that assumes host range trades off against fitness derived from a host species. In spite of such costs, a benefit to generalism may occur when the definitive host exhibits a large diet breadth, enhancing transmission of generalist parasites via consumption of a broad array of infected intermediate hosts. I develop a simple theoretical model to demonstrate how different host range infection strategies are differentially selected for across a gradient of definitive host diet breadth according to the cost of generalism. I then use a parasitic helminth–host database in conjunction with a food web database to show that diet breadth of definitive hosts promotes generalist infection strategies at the intermediate host level, indicating relatively low costs of parasite generalism among helminths.more » « less
-
Why parasites occur in certain hosts in certain locations has been a long-standing question among ecological and evolutionary parasitologists. Encounter and compatibility filters summarize the likelihood that a host and parasite will physically interact and establish an infection upon contact. Encounter and compatibility filters are not fixed and, among multiple locations, the abiotic environmental characteristics and biotic community composition that contribute to the filters often vary spatially and temporally. Abiotic variation may directly affect hosts or parasites —particularly parasites with one or more free-living stages— whereas the local biotic community may dilute or amplify parasite transmission. Unlike directly transmitted parasites, complex-life cycle parasites use multiple hosts, thus having life cycles that, we hypothesize, are highly susceptible to the effects of spatiotemporal environmental variation. We modeled infection probability relationships of endohelminths from post-metamorphic wood frogs (Rana [Lithobates] sylvatica) and northern leopard frogs (Rana pipiens) with wetland characteristics, landscape composition, and the anuran species within the local community. Parasites included complex-life cycle trematodes that use amphibians as definitive hosts (Haematoloechus spp., Glypthelmins quieta) or as intermediate hosts (Alaria sp., Neodiplostomum sp., echinostomatids, Lechriorchis) and nematodes with direct or indirect life cycles (Cosmocercoides, Oswaldocruzia). Although our results demonstrate that distributions of parasites with complex and direct life cycles are correlated with some abiotic and biotic characteristics of the environment, there were few general trends. Each parasite's distribution had its own unique relationship with wetland, landscape, and amphibian-community variables and there was overall low predictability for most species. One landscape feature — the number of wetlands within the vicinity of the site of amphibian capture — was commonly included in top models for leopard frogs and could be associated with how definitive hosts (e.g., amphibians, mammals, birds) and intermediate hosts (e.g., snails, odonates) use the landscape. The amphibian community at any given site also commonly affected infection probabilities, such that the local presence of other species tended to reduce infection probabilities in sampled frogs, lending support to the dilution effect at the landscape level. Our research highlights the need to consider spatiotemporal sampling, environmental variation, and host-community variation when studying parasite prevalence in any given component community.more » « less
