Title: Long-distance dispersal of pigeons and doves generated new ecological opportunities for host-switching and adaptive radiation by their parasites
Adaptive radiation is an important mechanism of organismal diversification and can be triggered by new ecological opportunities. Although poorly studied in this regard, parasites are an ideal group in which to study adaptive radiations because of their close associations with host species. Both experimental and comparative studies suggest that the ectoparasitic wing lice of pigeons and doves have adaptively radiated, leading to differences in body size and overall coloration. Here, we show that long-distance dispersal by dove hosts was central to parasite diversification because it provided new ecological opportunities for parasites to speciate after host-switching. We further show that among extant parasite lineages host-switching decreased over time, with cospeciation becoming the more dominant mode of parasite speciation. Taken together, our results suggest that host dispersal, followed by host-switching, provided novel ecological opportunities that facilitated adaptive radiation by parasites. more »« less
Haas, Genevieve M. S.; Hoberg, Eric P.; Cook, Joseph A.; Henttonen, Heikki; Makarikov, Arseny A.; Gallagher, Sarah R.; Dokuchaev, Nikolai E.; Galbreath, Kurt E.(
, Journal of Biogeography)
AbstractAim
We test the predictions of the Stockholm Paradigm, a synthesis of eco‐evolutionary theory explaining the nature of faunal assembly, host range and parasite diversification. Faunal diversification and assembly, manifested in patterns of host colonization, co‐adaptation and parasite speciation, are predicted to emerge as a consequence of alternating episodes of ecological disruption and stability. Specifically, for a diverse cestode genus (Arostrilepis), we evaluate the number and direction of Pleistocene dispersal events across Beringia, the number and relative timing of host colonization events and the relationship between host and parasite biogeographic histories and associations through time.
Location
Beringia and adjacent temperate to arctic biomes in North America and Eurasia.
Taxon
Arostrilepis(Cyclophyllidea: Hymenolepididae) and its rodent hosts.
Methods
Multi‐locus phylogenetic reconstruction and biogeographic ancestral range estimation.
Results
Arostrilepislineages crossed Beringia eastward into North America a minimum of four times and westward into Asia twice in association with temporally disjunct geographic expansions of three major tribes of cricetid rodents (Arvicolini, Myodini, Lemmini). Inferences of ancestral host associations support at least nine instances of host colonization involving shifts from one rodent tribe or family to another. Several previously unrecognized lineages ofArostrilepisare revealed.
Main conclusions
Consistent with expectations of the Stockholm Paradigm, episodes of intercontinental dispersal were both frequent in the history ofArostrilepisand preceded a majority of inferred host‐colonization events. Events of historical geographic expansion created numerous opportunities for development of novel host–parasite associations through ecological fitting, as parasites tracked historically conserved resources available across diverse host taxa. Beringia played a major role in shaping rodent/parasite assemblages by mediating dispersal between the northern continents during glacial episodes of the Pleistocene, rather than by serving as a zone of refugial isolation.
Community composition is driven by a few key assembly processes: ecological selection, drift and dispersal. Nested parasite communities represent a powerful study system for understanding the relative importance of these processes and their relationship with biological scale. Quantifying β‐diversity across scales and over time additionally offers mechanistic insights into the ecological processes shaping the distributions of parasites and therefore infectious disease.
To examine factors driving parasite community composition, we quantified the parasite communities of 959 amphibian hosts representing two species (the Pacific chorus frog, Pseudacris regilla and the California newt, Taricha torosa) sampled over 3 months from 10 ponds in California. Using additive partitioning, we estimated how much of regional parasite richness (γ‐diversity) was composed of within‐host parasite richness (α‐diversity) and turnover (β‐diversity) at three biological scales: across host individuals, across species and across habitat patches (ponds). We also examined how β‐diversity varied across time at each biological scale.
Differences among ponds comprised the majority (40%) of regional parasite diversity, followed by differences among host species (23%) and among host individuals (12%). Host species supported parasite communities that were less similar than expected by null models, consistent with ecological selection, although these differences lessened through time, likely due to high dispersal rates of infectious stages. Host individuals within the same population supported more similar parasite communities than expected, suggesting that host heterogeneity did not strongly impact parasite community composition and that dispersal was high at the individual host-level. Despite the small population sizes of within‐host parasite communities, drift appeared to play a minimal role in structuring community composition.
Dispersal and ecological selection appear to jointly drive parasite community assembly, particularly at larger biological scales. The dispersal ability of aquatic parasites with complex life cycles differs strongly across scales, meaning that parasite communities may predictably converge at small scales where dispersal is high, but may be more stochastic and unpredictable at larger scales. Insights into assembly mechanisms within multi‐host, multi‐parasite systems provide opportunities for understanding how to mitigate the spread of infectious diseases within human and wildlife hosts.
Moss, Wynne E.; McDevitt‐Galles, Travis; Calhoun, Dana M.; Johnson, Pieter T. J.; Cattadori, ed., Isabella(
, Journal of Animal Ecology)
Abstract
Community composition is driven by a few key assembly processes: ecological selection, drift and dispersal. Nested parasite communities represent a powerful study system for understanding the relative importance of these processes and their relationship with biological scale. Quantifyingβ‐diversity across scales and over time additionally offers mechanistic insights into the ecological processes shaping the distributions of parasites and therefore infectious disease.
To examine factors driving parasite community composition, we quantified the parasite communities of 959 amphibian hosts representing two species (the Pacific chorus frog,Pseudacris regillaand the California newt,Taricha torosa) sampled over 3 months from 10 ponds in California. Using additive partitioning, we estimated how much of regional parasite richness (γ‐diversity) was composed of within‐host parasite richness (α‐diversity) and turnover (β‐diversity) at three biological scales: across host individuals, across species and across habitat patches (ponds). We also examined howβ‐diversity varied across time at each biological scale.
Differences among ponds comprised the majority (40%) of regional parasite diversity, followed by differences among host species (23%) and among host individuals (12%). Host species supported parasite communities that were less similar than expected by null models, consistent with ecological selection, although these differences lessened through time, likely due to high dispersal rates of infectious stages. Host individuals within the same population supported more similar parasite communities than expected, suggesting that host heterogeneity did not strongly impact parasite community composition and that dispersal was high at the individual host-level. Despite the small population sizes of within‐host parasite communities, drift appeared to play a minimal role in structuring community composition.
Dispersal and ecological selection appear to jointly drive parasite community assembly, particularly at larger biological scales. The dispersal ability of aquatic parasites with complex life cycles differs strongly across scales, meaning that parasite communities may predictably converge at small scales where dispersal is high, but may be more stochastic and unpredictable at larger scales. Insights into assembly mechanisms within multi‐host, multi‐parasite systems provide opportunities for understanding how to mitigate the spread of infectious diseases within human and wildlife hosts.
Karvonen, Anssi; Wagner, Catherine E.; Selz, Oliver M.; Seehausen, Ole(
, Journal of Evolutionary Biology)
Abstract
Parasitism has been proposed as a factor in host speciation, as an agent affecting coexistence of host species in species‐rich communities and as a driver of post‐speciation diversification. Young adaptive radiations of closely related host species of varying ecological and genomic differentiation provide interesting opportunities to explore interactions between patterns of parasitism, divergence and coexistence of sympatric host species. Here, we explored patterns in ectoparasitism in a community of 16 fully sympatric cichlid species at Makobe Island in Lake Victoria, a model system of vertebrate adaptive radiation. We asked whether host niche, host abundance or host genetic differentiation explains variation in infection patterns. We found significant differences in infections, the magnitude of which was weakly correlated with the extent of genomic divergence between the host species, but more strongly with the main ecological gradient, water depth. These effects were most evident with infections ofCichlidogyrusmonogeneans, whereas the only host species with a strictly crevice‐dwelling niche,Pundamilia pundamilia, deviated from the general negative relationship between depth and parasitism. In accordance with the Janzen–Connell hypothesis, we also found that host abundance tended to be positively associated with infections in some parasite taxa. Data on thePundamiliasister species pairs from three other islands with variable degrees of habitat (crevice) specialization suggested that the lower parasite abundance ofP. pundamiliaat Makobe could result from both habitat specialization and the evolution of specific resistance. Our results support influences of host genetic differentiation and host ecology in determining infections in this diverse community of sympatric cichlid species.
Although parasites are known to have various effects on their hosts, we know little about their role in the assembly of diversifying host populations. Using an experimental bacterium (Pseudomonas fluorescens SBW25)-bacteriophage (ϕ2) system, we show that earlier parasite arrival significantly reduced the repeatability of host diversification. Earlier parasite arrival amplified the priority effects associated with the stochastic emergence of novel SBW25 phenotypes, translating into greater historical contingency in SBW25 diversification. Our results highlight the important role of parasite-host interactions in driving host adaptive radiation.
Boyd, Bret M., Nguyen, Nam-Phuong, Allen, Julie M., Waterhouse, Robert M., Vo, Kyle B., Sweet, Andrew D., Clayton, Dale H., Bush, Sarah E., Shapiro, Michael D., and Johnson, Kevin P. Long-distance dispersal of pigeons and doves generated new ecological opportunities for host-switching and adaptive radiation by their parasites. Retrieved from https://par.nsf.gov/biblio/10345579. Proceedings of the Royal Society B: Biological Sciences 289.1970 Web. doi:10.1098/rspb.2022.0042.
Boyd, Bret M., Nguyen, Nam-Phuong, Allen, Julie M., Waterhouse, Robert M., Vo, Kyle B., Sweet, Andrew D., Clayton, Dale H., Bush, Sarah E., Shapiro, Michael D., & Johnson, Kevin P. Long-distance dispersal of pigeons and doves generated new ecological opportunities for host-switching and adaptive radiation by their parasites. Proceedings of the Royal Society B: Biological Sciences, 289 (1970). Retrieved from https://par.nsf.gov/biblio/10345579. https://doi.org/10.1098/rspb.2022.0042
Boyd, Bret M., Nguyen, Nam-Phuong, Allen, Julie M., Waterhouse, Robert M., Vo, Kyle B., Sweet, Andrew D., Clayton, Dale H., Bush, Sarah E., Shapiro, Michael D., and Johnson, Kevin P.
"Long-distance dispersal of pigeons and doves generated new ecological opportunities for host-switching and adaptive radiation by their parasites". Proceedings of the Royal Society B: Biological Sciences 289 (1970). Country unknown/Code not available. https://doi.org/10.1098/rspb.2022.0042.https://par.nsf.gov/biblio/10345579.
@article{osti_10345579,
place = {Country unknown/Code not available},
title = {Long-distance dispersal of pigeons and doves generated new ecological opportunities for host-switching and adaptive radiation by their parasites},
url = {https://par.nsf.gov/biblio/10345579},
DOI = {10.1098/rspb.2022.0042},
abstractNote = {Adaptive radiation is an important mechanism of organismal diversification and can be triggered by new ecological opportunities. Although poorly studied in this regard, parasites are an ideal group in which to study adaptive radiations because of their close associations with host species. Both experimental and comparative studies suggest that the ectoparasitic wing lice of pigeons and doves have adaptively radiated, leading to differences in body size and overall coloration. Here, we show that long-distance dispersal by dove hosts was central to parasite diversification because it provided new ecological opportunities for parasites to speciate after host-switching. We further show that among extant parasite lineages host-switching decreased over time, with cospeciation becoming the more dominant mode of parasite speciation. Taken together, our results suggest that host dispersal, followed by host-switching, provided novel ecological opportunities that facilitated adaptive radiation by parasites.},
journal = {Proceedings of the Royal Society B: Biological Sciences},
volume = {289},
number = {1970},
author = {Boyd, Bret M. and Nguyen, Nam-Phuong and Allen, Julie M. and Waterhouse, Robert M. and Vo, Kyle B. and Sweet, Andrew D. and Clayton, Dale H. and Bush, Sarah E. and Shapiro, Michael D. and Johnson, Kevin P.},
}
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