Rapid evolution of virulence leading to host extinction under host-parasite coevolution

ABSTRACT Pathogens vectored by nematodes pose serious agricultural, economic, and health threats; however, little is known of the ecological and evolutionary aspects of pathogen transmission by nematodes. Here we describe a novel model system with two trophic levels, bacteriophages and nematodes, each of which competes for bacteria. We demonstrate for the first time that nematodes are capable of transmitting phages between spatially distinct patches of bacteria. This model system has considerable advantages, including the ease of maintenance and manipulation at the laboratory bench, the ability to observe many generations in short periods, and the capacity to freeze evolved strains for later comparison to their ancestors. More generally, experimental studies of complex multispecies interactions, host-pathogen coevolution, disease dynamics, and the evolution of virulence may benefit from this model system because current models (e.g., chickens, mosquitoes, and malaria parasites) are costly to maintain, are difficult to manipulate, and require considerable space. Our initial explorations centered on independently assessing the impacts of nematode, bacterium, and phage population densities on virus migration between host patches. Our results indicated that virus transmission increases with worm density and host bacterial abundance; however, transmission decreases with initial phage abundance, perhaps because viruses eliminate available hosts before migration can occur. We discuss the microbial growth dynamics that underlie these results, suggest mechanistic explanations for nematode transmission of phages, and propose intriguing possibilities for future research.

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WITHIN-HOST PARASITE DYNAMICS, EMERGING TRADE-OFF, AND EVOLUTION OF VIRULENCE WITH IMMUNE SYSTEM

Evolution ◽

10.1554/02-667 ◽

2003 ◽

Vol 57 (7) ◽

pp. 1489 ◽

Cited By ~ 4

Author(s):

Jean-Baptiste André ◽

Jean-Baptiste Ferdy ◽

Bernard Godelle

Keyword(s):

Immune System ◽

Trade Off ◽

Evolution Of Virulence ◽

Host Parasite ◽

Parasite Dynamics

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Rapid evolution and ecological host-parasite dynamics

Ecology Letters ◽

10.1111/j.1461-0248.2006.00995.x ◽

2006 ◽

Vol 10 (1) ◽

pp. 44-53 ◽

Cited By ~ 152

Author(s):

Meghan A. Duffy ◽

Lena Sivars-Becker

Keyword(s):

Rapid Evolution ◽

Host Parasite ◽

Parasite Dynamics

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The ghost of hosts past: impacts of host extinction on parasite specificity

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2020.0351 ◽

2021 ◽

Vol 376 (1837) ◽

pp. 20200351 ◽

Cited By ~ 4

Author(s):

Maxwell J. Farrell ◽

Andrew W. Park ◽

Clayton E. Cressler ◽

Tad Dallas ◽

Shan Huang ◽

...

Keyword(s):

Host Specificity ◽

Disease Ecology ◽

Parasite Species ◽

Biodiversity Loss ◽

Virulence Evolution ◽

Host Phylogeny ◽

Parasite Biodiversity ◽

Host Parasite ◽

The Impact ◽

Host Extinction

A growing body of research is focused on the extinction of parasite species in response to host endangerment and declines. Beyond the loss of parasite species richness, host extinction can impact apparent parasite host specificity, as measured by host richness or the phylogenetic distances among hosts. Such impacts on the distribution of parasites across the host phylogeny can have knock-on effects that may reshape the adaptation of both hosts and parasites, ultimately shifting the evolutionary landscape underlying the potential for emergence and the evolution of virulence across hosts. Here, we examine how the reshaping of host phylogenies through extinction may impact the host specificity of parasites, and offer examples from historical extinctions, present-day endangerment, and future projections of biodiversity loss. We suggest that an improved understanding of the impact of host extinction on contemporary host–parasite interactions may shed light on core aspects of disease ecology, including comparative studies of host specificity, virulence evolution in multi-host parasite systems, and future trajectories for host and parasite biodiversity. This article is part of the theme issue ‘Infectious disease macroecology: parasite diversity and dynamics across the globe’.

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A theoretical model of the evolution of virulence in sexually transmitted HIV/AIDS

Revista de Saúde Pública ◽

10.1590/s0034-89101999000400002 ◽

1999 ◽

Vol 33 (4) ◽

pp. 329-333 ◽

Cited By ~ 4

Author(s):

FAB Coutinho ◽

E Massad ◽

RX Menezes ◽

MN Burattini

Keyword(s):

Sexual Activity ◽

Virulent Strain ◽

Host Population ◽

Sexual Partners ◽

High Rate ◽

Potential Influence ◽

Sexually Transmitted ◽

Evolution Of Virulence ◽

The Subject ◽

Host Parasite

INTRODUCTION: The evolution of virulence in host-parasite relationships has been the subject of several publications. In the case of HIV virulence, some authors suggest that the evolution of HIV virulence correlates with the rate of acquisition of new sexual partners. In contrast some other authors argue that the level of HIV virulence is independent of the sexual activity of the host population. METHODS: Provide a mathematical model for the study of the potential influence of human sexual behaviour on the evolution of virulence of HIV is provided. RESULTS: The results indicated that, when the probability of acquisition of infection is a function both of the sexual activity and of the virulence level of HIV strains, the evolution of HIV virulence correlates positively with the rate of acquisition of new sexual partners. CONCLUSION: It is concluded that in the case of a host population with a low (high) rate of exchange of sexual partners the evolution of HIV virulence is such that the less (more) virulent strain prevails.

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Factors affecting the evolution of virulence: nematode parasites of fig wasps as a case study

Parasitology ◽

10.1017/s0031182000075880 ◽

1995 ◽

Vol 111 (S1) ◽

pp. S179-S191 ◽

Cited By ~ 51

Author(s):

E. A. Herre

Keyword(s):

Horizontal Transmission ◽

Host Population ◽

Lifetime Reproductive Success ◽

Evolutionary Relationships ◽

Parameter Estimates ◽

Fig Wasps ◽

Evolution Of Virulence ◽

Wide Range ◽

The Individual ◽

Host Parasite

SUMMARYThe natural history of fig-pollinating wasps and their associated species-specific nematodes allows the measurement of many parameters which are relevant to testing hypotheses concerning host-parasite ecology and evolution. Within fig wasps species, it is possible to estimate lifetime reproductive success of foundress wasps as a function of presence or absence of nematode parasitism (virulence). Across species, there is a wide range of host population structures which, in turn, results in a range of opportunities for either horizontal or vertical nematode transmission. Therefore, estimates of virulence can be related to opportunities for transmission across a group of closely related hosts and their parasites. Further, the dynamics of the nematode infections over ecological and short-term evolutionary timescales can be monitored, giving added insight into the interpretation of the virulence estimates. Moreover, several scales of longer term evolutionary relationships are either known directly from fossil evidence or can be inferred from molecular data, providing deeper temporal context for the observed patterns. This combination of attributes permits detailed testing of hypotheses concerning the factors that potentially influence the evolution of virulence in host-parasite systems, and further, population and simulation models of the system that incorporate the parameter estimates can clarify the interpretation of how those factors act. There is little evidence suggesting that intermediate and long-term evolutionary relationships explain current levels of virulence. That is, it appears that virulence can change rapidly relative to speciation events, and that the nematodes do not tend to become ‘benign over time’. Instead, it appears that host population structure can influence the evolution of parasite virulence by affecting the relative opportunities for horizontal to vertical transmission, which, in turn, influences the relative costs and benefits of virulence to the nematodes. At one level, increased opportunities for horizontal transmission decouple the reproductive interests of the individual nematodes from those of the individual hosts that they are directly parasitizing, thereby reducing the cost of virulence to individual nematodes. At another level, increased opportunities of horizontal transmission also increases the relative frequency of hosts infected by multiple strains of nematodes. This promotes the evolution of more virulent forms by increasing the relative importance of within-host competition among nematode strains, thereby favouring strains that ‘eat more host sooner’. An interesting property of the fig-nematode systems is that the proportion of infected hosts does not change dramatically through time. This finding implies that there can be considerable negative effects on survival of infected hosts in addition to the previously documented reductions in fecundity of infected foundresses, because the latter are insufficient to account for the observed stability of wasp infection rates.

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Identification of an ancient endogenous retrovirus, predating the divergence of the placental mammals

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2012.0503 ◽

2013 ◽

Vol 368 (1626) ◽

pp. 20120503 ◽

Cited By ~ 29

Author(s):

Adam Lee ◽

Alison Nolan ◽

Jason Watson ◽

Michael Tristem

Keyword(s):

Rapid Evolution ◽

Endogenous Retrovirus ◽

Arms Race ◽

Endogenous Retroviruses ◽

Selfish Genetic Elements ◽

Host Parasite Interactions ◽

Combined Use ◽

Minimum Age ◽

Host Parasite ◽

First Time

The evolutionary arms race between mammals and retroviruses has long been recognized as one of the oldest host–parasite interactions. Rapid evolution rates in exogenous retroviruses have often made accurate viral age estimations highly problematic. Endogenous retroviruses (ERVs), however, integrate into the germline of their hosts, and are subjected to their evolutionary rates. This study describes, for the first time, a retroviral orthologue predating the divergence of placental mammals, giving it a minimum age of 104–110 Myr. Simultaneously, other orthologous selfish genetic elements (SGEs), inserted into the ERV sequence, provide evidence for the oldest individual mammalian-wide interspersed repeat and medium-reiteration frequency interspersed repeat mammalian repeats, with the same minimum age. The combined use of shared SGEs and reconstruction of viral orthologies defines new limits and increases maximum ‘lookback’ times, with subsequent implications for the field of paleovirology.

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Immune defence, parasite evasion strategies and their relevance for ‘macroscopic phenomena’ such as virulence

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2008.0157 ◽

2008 ◽

Vol 364 (1513) ◽

pp. 85-98 ◽

Cited By ~ 105

Author(s):

Paul Schmid-Hempel

Keyword(s):

Immune Evasion ◽

Life History Theory ◽

Evolutionary Ecology ◽

Parasite Clearance ◽

Multiple Infections ◽

Parasite Fitness ◽

Host Parasite Interactions ◽

Evolution Of Virulence ◽

Host Parasite ◽

Insight Into

The discussion of host–parasite interactions, and of parasite virulence more specifically, has so far, with a few exceptions, not focused much attention on the accumulating evidence that immune evasion by parasites is not only almost universal but also often linked to pathogenesis, i.e. the appearance of virulence. Now, the immune evasion hypothesis offers a deeper insight into the evolution of virulence than previous hypotheses. Sensitivity analysis for parasite fitness and life-history theory shows promise to generate a more general evolutionary theory of virulence by including a major element, immune evasion to prevent parasite clearance from the host. Also, the study of dose–response relationships and multiple infections should be particularly illuminating to understand the evolution of virulence. Taking into account immune evasion brings immunological processes to the core of understanding the evolution of parasite virulence and for a range of related issues such as dose, host specificity or immunopathology. The aim of this review is to highlight the mechanism underlying immune evasion and to discuss possible consequences for the evolutionary ecology analysis of host–parasite interactions.

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Coevolution of virulence and immunosuppression in multiple infections

10.1101/149211 ◽

2017 ◽

Author(s):

Tsukushi Kamiya ◽

Nicole Mideo ◽

Samuel Alizon

Keyword(s):

Evolutionary Biology ◽

Adaptive Dynamics ◽

Multiple Infections ◽

Research Attention ◽

Background Mortality ◽

Evolution Of Virulence ◽

Duration Of Infection ◽

Peer Community ◽

The Cost ◽

Host Parasite

AbstractThis preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (http://dx.doi.org/10.24072/pci.evolbiol.100043). Many components of host-parasite interactions have been shown to affect the way virulence (i.e., parasite-induced harm to the host) evolves. However, coevolution of multiple parasite traits is often neglected. We explore how an immunosuppressive mechanism of parasites affects and coevolves with virulence through multiple infections. Applying the adaptive dynamics framework to epidemiological models with coinfection, we show that immunosuppression is a double-edged-sword for the evolution of virulence. On one hand, it amplifies the adaptive benefit of virulence by increasing the abundance of coinfections through epidemiological feedbacks. On the other hand, immunosuppression hinders host recovery, prolonging the duration of infection and elevating the cost of killing the host. The balance between the cost and benefit of immunosuppression varies across different background mortality rates of hosts. In addition, we find that immunosuppression evolution is influenced considerably by the precise trade-off shape determining the effect of immunosuppression on host recovery and susceptibility to further infection. These results demonstrate that the evolution of virulence is shaped by immunosuppression while highlighting that the evolution of immune evasion mechanisms deserves further research attention.

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