Virulence, the degree to which a pathogen harms its host, is an important but poorly understood aspect of host-pathogen interactions. Virulence is not static, instead depending on ecological context and potentially evolving rapidly. For instance, at the start of an epidemic, when susceptible hosts are plentiful, pathogens may evolve increased virulence if this maximizes their intrinsic growth rate. However, if host density declines during an epidemic, theory predicts evolution of reduced virulence. Although well-studied theoretically, there is still little empirical evidence for virulence evolution in epidemics, especially in natural settings with native host and pathogen species. Here, we used a combination of field observations and lab assays in the
Ecological context influences evolution in host-parasite interactions: insights from the Daphnia-parasite model system
Parasites exert strong selective pressure on their hosts, and many hosts can evolve rapidly in response. As such, host-parasite interactions have a special place in the study of contemporary evolution. However, these interactions are often considered in isolation from the ecological contexts in which they occur. Here we review different ways in which the ecological context of host-parasite interactions can modulate their evolutionary outcomes in important and sometimes unexpected ways. Specifically, we highlight how predation, competition, and abiotic factors change the outcome of contemporary evolution for both hosts and parasites. In doing so, we focus on insights gained from the Daphnia-microparasite system. This system has emerged as a model system for understanding the ecology and evolution of host-parasite interactions, and has provided important insights into how ecological context influences contemporary evolution.
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- NSF-PAR ID:
- 10180123
- Date Published:
- Journal Name:
- Evolution in Action: Past, Present and Future
- Page Range / eLocation ID:
- 289-307
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Daphnia -Pasteuria model system to look for evidence of virulence evolution in nature. We monitored a large, naturally occurring outbreak ofPasteuria ramosa inDaphnia dentifera , where infection prevalence peaked at ~ 40% of the population infected and host density declined precipitously during the outbreak. In controlled infections in the lab, lifespan and reproduction of infected hosts was lower than that of unexposed control hosts and of hosts that were exposed but not infected. We did not detect any significant changes in host resistance or parasite infectivity, nor did we find evidence for shifts in parasite virulence (quantified by host lifespan and number of clutches produced by hosts). However, over the epidemic, the parasite evolved to produce significantly fewer spores in infected hosts. While this finding was unexpected, it might reflect previously quantified tradeoffs: parasites in high mortality (e.g., high predation) environments shift from vegetative growth to spore production sooner in infections, reducing spore yield. Future studies that track evolution of parasite spore yield in more populations, and that link those changes with genetic changes and with predation rates, will yield better insight into the drivers of parasite evolution in the wild. -
null (Ed.)A wealth of information about how parasites interact with their hosts already exists in collections, scientific publications, specialized databases, and grey literature. The US National Science Foundation-funded Terrestrial Parasite Tracker Thematic Collection Network (TPT) project began in 2019 to help build a comprehensive picture of arthropod ectoparasites including the evolution of these parasite-host biotic associations, distributions, and the ecological interactions of disease vectors. TPT is a network of biodiversity collections whose data can assist scientists, educators, land managers, and policymakers to better understand the complex relationship between hosts and parasites including emergent properties that may explain the causes and frequency of human and wildlife pathogens. TPT member collections make their association information easier to access via Global Biotic Interactions (GloBI, Poelen et al. 2014), which is periodically archived through Zenodo to track progress in the TPT project. TPT leverages GloBI's ability to index biotic associations from specimen occurrence records that come from existing management systems (e.g., Arctos, Symbiota, EMu, Excel, MS Access) to avoid having to completely rework existing, or build new, cyber-infrastructures before collections can share data. TPT-affiliated collection managers use collection-specific translation tables to connect their verbatim (or original) terms used to describe associations (e.g., "ex", "found on", "host") to their interpreted, machine-readable terms in the OBO Relations Ontology (RO). These interpreted terms enable searches across previously siloed association record sets, while the original verbatim values remain accessible to help retain provenance and allow for interpretation improvements. TPT is an ambitious project, with the goal to database label data from over 1.2 million specimens of arthropod parasites of vertebrates coming from 22 collections across North America. In the first year of the project, the TPT collections created over 73,700 new records and 41,984 images. In addition, 17 TPT data providers and three other collaborators shared datasets that are now indexed by GloBI, visible on the TPT GloBI project page. These datasets came from collection specimen occurrence records and literature sources. Two TPT data archives that capture and preserve the changes in the data coming from TPT to GloBI were published through Zenodo (Poelen et al. 2020a, Poelen et al. 2020b). The archives document the changes in how data are shared by collections including the biotic association data format and quantity of data captured. The Poelen et al. 2020b report included all TPT collections and biotic interactions from Arctos collections in VertNet and the Symbiota Collection of Arthropods Network (SCAN). The total number of interactions included in this report was 376,671 records (500,000 interactions is the overall goal for TPT). In addition, close coordination with TPT collection data managers including many one-on-one conversations, a workshop, and a webinar (Sullivan et al. 2020) was conducted to help guide the data capture of biotic associations. GloBI is an effective tool to help integrate biotic association data coming from occurrence records into an openly accessible, global, linked view of existing species interaction records. The results gleaned from the TPT workshop and Zenodo data archives demonstrate that minimizing changes to existing workflows allow for custom interpretation of collection-specific interaction terms. In addition, including collection data managers in the development of the interaction term vocabularies is an important part of the process that may improve data sharing and the overall downstream data quality.more » « less
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Social interactions with conspecifics are key to the fitness of most animals and, through the transmission opportunities they provide, are also key to the fitness of their parasites. As a result, research to date has largely focused on the role of host social behavior in imposing selection on parasites, particularly their virulence and transmission phenotypes. However, host social behavior also influences the distribution of parasites among hosts, with implications for their evolution through non-random mating, gene flow, and genetic drift, and thus ability to respond to that selection. Here, we review the paucity of empirical studies on parasites, and draw from empirical studies of free-living organisms and population genetic theory to propose several mechanisms by which host social behavior potentially drives parasite evolution through these less-well studied mechanisms. We focus on the guppy host and Gyrodactylus (Monogenea) ectoparasitic flatworm system and follow a spatially hierarchical outline to highlight that social behavior varies between individuals, and between host populations across the landscape, generating a mosaic of ecological and evolutionary outcomes for their infecting parasites. We argue that the guppy-Gyrodactylus system presents a unique opportunity to address this fundamental knowledge gap in our understanding of the connection between host social behavior and parasite evolution. Individual differences in host social behavior generates fine-scale changes in the spatial distribution of parasite genotypes, shape the size, and diversity of their infecting parasite populations and may generate non-random mating on, and non-random transmission between hosts. While at population and metapopulation level, variation in host social behavior interacts with landscape structure to affect parasite gene flow, effective population size, and genetic drift to alter the coevolutionary potential of local adaptation.more » « less
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Abstract The relationships between avian brood parasites and their hosts are widely recognised as model systems for studying coevolution. However, while most brood parasites are known to parasitise multiple species of host and hosts are often subject to parasitism by multiple brood parasite species, the examination of multispecies interactions remains rare. Here, we compile data on all known brood parasite–host relationships and find that complex brood parasite–host systems, where multiple species of brood parasites and hosts coexist and interact, are globally commonplace. By examining patterns of past research, we outline the disparity between patterns of network complexity and past research emphases and discuss factors that may be associated with these patterns. Drawing on insights gained from other systems that have embraced a multispecies framework, we highlight the potential benefits of considering brood parasite–host interactions as ecological networks and brood parasitism as a model system for studying multispecies interactions. Overall, our results provide new insights into the diversity of these relationships, highlight the stark mismatch between past research efforts and global patterns of network complexity, and draw attention to the opportunities that more complex arrangements offer for examining how species interactions shape global patterns of biodiversity.
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null (Ed.)Abstract An animal's social behaviour both influences and changes in response to its parasites. Here we consider these bidirectional links between host social behaviours and parasite infection, both those that occur from ecological vs evolutionary processes. First, we review how social behaviours of individuals and groups influence ecological patterns of parasite transmission. We then discuss how parasite infection, in turn, can alter host social interactions by changing the behaviour of both infected and uninfected individuals. Together, these ecological feedbacks between social behaviour and parasite infection can result in important epidemiological consequences. Next, we consider the ways in which host social behaviours evolve in response to parasites, highlighting constraints that arise from the need for hosts to maintain benefits of sociality while minimizing fitness costs of parasites. Finally, we consider how host social behaviours shape the population genetic structure of parasites and the evolution of key parasite traits, such as virulence. Overall, these bidirectional relationships between host social behaviours and parasites are an important yet often underappreciated component of population-level disease dynamics and host–parasite coevolution.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Conference Paper:
- https://doi.org/https://doi.org/10.1007/978-3-030-39831-6_21
