An official website of the United States government
Abstract Despite the ubiquitous nature of parasitism, how parasitism alters the outcome of host–species interactions such as competition, mutualism and predation remains unknown. Using a phylogenetically informed meta‐analysis of 154 studies, we examined how the mean and variance in the outcomes of species interactions differed between parasitized and non‐parasitized hosts. Overall, parasitism did not significantly affect the mean or variance of host–species interaction outcomes, nor did the shared evolutionary histories of hosts and parasites have an effect. Instead, there was considerable variation in outcomes, ranging from strongly detrimental to strongly beneficial for infected hosts. Trophically‐transmitted parasites increased the negative effects of predation, parasites increased and decreased the negative effects of interspecific competition for parasitized and non‐parasitized heterospecifics, respectively, and parasites had particularly strong negative effects on host species interactions in freshwater and marine habitats, yet were beneficial in terrestrial environments. Our results illuminate the diverse ways in which parasites modify critical linkages in ecological networks, implying that whether the cumulative effects of parasitism are considered detrimental depends not only on the interactions between hosts and their parasites but also on the many other interactions that hosts experience.
more »
« less
Parasitism shapes selection by drastically reducing host fitness and increasing host fitness variation
Determining the effects of parasites on host reproduction is key to understanding how parasites affect the underpinnings of selection on hosts. Although infection is expected to be costly, reducing mean fitness, infection could also increase variation in fitness costs among hosts, both of which determine the potential for selection on hosts. To test these ideas, we used a phylogenetically informed meta-analysis of 118 studies to examine how changes in the mean and variance in the outcome of reproduction differed between parasitized and non-parasitized hosts. We found that parasites had severe negative effects on mean fitness, with parasitized hosts suffering reductions in fecundity, viability and mating success. Parasite infection also increased variance in reproduction, particularly fecundity and offspring viability. Surprisingly, parasites had similar effects on viability when either the male or female was parasitized. These results not only provide the first synthetic, comparative, and quantitative summary of the strong deleterious effects of parasites on host reproductive fitness, but also reveal a consistent role for parasites in shaping the opportunity for selection.
more »
« less
- Award ID(s):
- 1748945
- PAR ID:
- 10409375
- Date Published:
- Journal Name:
- Biology Letters
- Volume:
- 18
- Issue:
- 11
- ISSN:
- 1744-957X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Li_Richter, Xiang-Yi; Jain, Kavita (Ed.)Abstract There is overwhelming evidence that the microbiome can be important to host physiology and fitness. As such, there is interest in and some theoretical work on understanding when hosts and microbiomes (co)evolve so that microbes benefit hosts and hosts favour beneficial microbes. However, the outcome of evolution likely depends on how microbes benefit hosts. Here, we use adaptive dynamics to investigate how host and symbiont evolution depend on whether symbionts increase host lifespan or host reproduction in a simple model of host and symbiont dynamics. In addition, we investigate 2 ways hosts release (and transmit) symbionts: by releasing symbionts steadily during their lifetime or by releasing them at reproduction, potentially increasing symbionts’ chances of infecting the host’s offspring. The former is strict horizontal transmission, whereas the latter is also a form of indirect or “pseudovertical” transmission. Our first key result is that the evolution of symbionts that benefit host fecundity requires pseudovertical transmission, while the evolution of symbionts that benefit host lifespan does not. Furthermore, our second key result is that when investing in host benefits is costly to the free-living symbiont stage, intermediate levels of pseudovertical transmission are needed for selection to favour beneficial symbionts. This is true regardless of fitness effects because release at reproduction increases the free-living symbiont population, which increases competition for hosts. Consequently, hosts could evolve away from traits that favour beneficial symbionts. Generally, our work emphasizes the importance of different forms of vertical transmission and fitness benefits in host, microbiome, and holobiont evolution as highlighted by our prediction that the evolution of fecundity-increasing symbionts requires parent-to-offspring transmission.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
-
Li_Richter, Xiang-Yi; Mullon, Charles (Ed.)Abstract Given their ubiquity in nature and their importance to human and agricultural health, it is important to gain a better understanding of the drivers of the evolution of infectious disease. Across vertebrates, invertebrates, and plants, defence mechanisms can be expressed either constitutively (always present and costly) or induced (activated and potentially costly only upon infection). Theory has shown that this distinction has important implications to the evolution of defence due to differences in their impact on both individual fitness and the feedback of the population-level epidemiological outcomes such as prevalence. However, despite the fact that pathogens evolve in response to host immunity and that this can have important implications to the evolution of host defence, the implications of coevolution on constitutive and induced immunity have not been examined. Here we show theoretically how and when incorporating host-parasite coevolution between host defences and parasite growth strategies plays an important role in determining the optimum outcome. A key result is that whether the parasite affects host reproduction critically impacts host-parasite coevolution; when the parasite impacts fecundity, selection on the host is largely geared towards minimizing reproductive costs, through reducing investment in reproductively costly constitutive defence when the parasite prevalence is low, but also by investing in immunity to avoid infection or recover when prevalence is high. Our work emphasizes the importance of coevolution and epidemiological feedbacks to the coevolution of hosts and parasites and provides testable predictions of the determinants of constitutive verses induced defence.more » « less
-
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
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1098/rsbl.2022.0323
