When a species colonizes a new range, it can escape enemies found in its original range. Examples of enemy escape abound for invasive species, but are rare for climate migrants, which are populations of a species that colonize a new range due to climate-driven range shifts or expansions. The fiddler crab Minuca (= Uca ) pugnax is found in the intertidal salt marshes of the US east coast. It recently expanded its range north into the Gulf of Maine as a result of ocean warming. We tested the hypothesis that M. pugnax had escaped its parasite enemies. Parasite richness and trematode intensity were lower in populations in the expanded range than in populations in the historical range, but infection prevalence did not differ. Although M. pugnax escaped most of its historical parasites when it migrated northward, it was infected with black-gill lamellae (indicative of Synophrya hypertrophica ), which was found in the historical range, and with the trematode Odhneria cf. odhneri , which was not found in the historical range. To our knowledge, this is the first time that O. cf. odhneri has been reported in fiddler crabs. These results demonstrate that although M. pugnax escaped some of its historical parasites when it expanded its range, it appears to have gained a new parasite ( O. cf. odhneri ) in the expanded range. Overall, our results demonstrate that climate migrants can escape their enemies despite colonizing habitats adjacent to their enemy-filled historical range.
more »
« less
Influences of land use and ecological variables on trematode prevalence and intensity at the salt marsh‐upland ecotone
Abstract Human‐altered shorelines make up approximately 14% of the coastline in the United States, with consequences for marsh ecosystems ranging from altered physical and biological variables, to direct loss of intertidal marsh habitat, to diminished land–sea connectivity. Trophically transmitted parasites that require connectivity between upland host species and marsh host species to complete their complex lifecycles could be particularly sensitive to the effects of shoreline alterations. They can additionally respond to gradients in natural physical and biological factors, including the host communities, that are often sharp at the land–sea ecotone. Across 27 salt marshes over 45 km, we evaluated the effects of environmental variables and three types of land use (undeveloped; single‐house adjacent to the marsh with small‐scale shoreline armoring; and single‐house adjacent to the marsh without shoreline armoring), on infection prevalence and intensity of the trematodeMicrophallus basodactylophallusin its second intermediate crab host,Minuca pugnax. The first intermediate hosts ofM. basodactylophallusare Hydrobiid snail species that are obligate marsh residents, while the definitive hosts are terrestrial rodents and raccoons. Thus, trematode transmission must depend on cross‐boundary movement by the definitive hosts. We found that although there was a trend of lower infection prevalence at undeveloped forested sites, there was no significant effect of adjacent land development on infection prevalence or intensity. Instead host, biotic and abiotic factors were correlated with infection; namely, largerM. pugnaxhad higher prevalence and intensity ofM. basodactylophallus, and higher soil moisture and lower density of the ribbed mussel (Geukensia demissa) were associated with increasedM. basodactylophallusprevalence. The small, indirect influence of upland development suggests that movement of definite hosts across the ecotone may be largely unaffected. Further, the robust trematode levels signify the ecosystem and the species interactions, upon which its complex lifecycle depends, are largely intact.
more »
« less
- Award ID(s):
- 1832178
- PAR ID:
- 10450128
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Ecosphere
- Volume:
- 12
- Issue:
- 8
- ISSN:
- 2150-8925
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
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
-
Abstract Manipulation of host phenotypes by parasites is hypothesized to be an adaptive strategy enhancing parasite transmission across hosts and generations. Characterizing the molecular mechanisms of manipulation is important to advance our understanding of host–parasite coevolution. The trematode (Levinseniella byrdi) is known to alter the colour and behaviour of its amphipod host (Orchestia grillus) presumably increasing predation of amphipods which enhances trematode transmission through its life cycle. We sampled 24 infected and 24 uninfected amphipods from a salt marsh in Massachusetts to perform differential gene expression analysis. In addition, we constructed novel genomic tools forO. grillusincluding a de novo genome and transcriptome. We discovered that trematode infection results in upregulation of amphipod transcripts associated with pigmentation and detection of external stimuli, and downregulation of multiple amphipod transcripts implicated in invertebrate immune responses, such as vacuolar ATPase genes. We hypothesize that suppression of immune genes and the altered expression of genes associated with coloration and behaviour may allow the trematode to persist in the amphipod and engage in further biochemical manipulation that promotes transmission. The genomic tools and transcriptomic analyses reported provide new opportunities to discover how parasites alter diverse pathways underlying host phenotypic changes in natural populations.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
-
null (Ed.)A key challenge surrounding ongoing climate shifts is to identify how they alter species interactions, including those between hosts and parasites. Because transmission often occurs during critical time windows, shifts in the phenology of either taxa can alter the likelihood of interaction or the resulting pathology. We quantified how phenological synchrony between vulnerable stages of an amphibian host ( Pseudacris regilla ) and infection by a pathogenic trematode ( Ribeiroia ondatrae ) determined infection prevalence, parasite load and host pathology. By tracking hosts and parasite infection throughout development between low- and high-elevation regions (San Francisco Bay Area and the Southern Cascades (Mt Lassen)), we found that when phenological synchrony was high (Bay Area), each established parasite incurred a 33% higher probability of causing severe limb malformations relative to areas with less synchrony (Mt Lassen). As a result, hosts in the Bay Area had up to a 50% higher risk of pathology even while controlling for the mean infection load. Our results indicate that host–parasite interactions and the resulting pathology were the joint product of infection load and phenological synchrony, highlighting the sensitivity of disease outcomes to forecasted shifts in climate.more » « less
An official website of the United States government
