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1.
Parasitology ; 145(6): 770-774, 2018 05.
Article in English | MEDLINE | ID: mdl-28502267

ABSTRACT

Competition between parasite species or genotypes can play an important role in the establishment of parasites in new host populations. Here, we investigate a mechanism by which a rare parasite is unable to establish itself in a host population if a common resident parasite is already present (a 'priority effect'). We develop a simple epidemiological model and show that a rare parasite genotype is unable to invade if coinfecting parasite genotypes inhibit each other's transmission more than expected from simple resource partitioning. This is because a rare parasite is more likely to be in multiply-infected hosts than the common genotype, and hence more likely to pay the cost of reduced transmission. Experiments competing interfering clones of bacteriophage infecting a bacterium support the model prediction that the clones are unable to invade each other from rare. We briefly discuss the implications of these results for host-parasite ecology and (co)evolution.


Subject(s)
Host-Parasite Interactions , Parasites/physiology , Animals , Bacteria/genetics , Bacteria/virology , Bacteriophages/genetics , Bacteriophages/physiology , Genotype , Microbial Interactions , Models, Statistical , Parasites/genetics
2.
Philos Trans R Soc Lond B Biol Sci ; 372(1719)2017 May 05.
Article in English | MEDLINE | ID: mdl-28289251

ABSTRACT

This article reviews research on the evolutionary mechanisms leading to different transmission modes. Such modes are often under genetic control of the host or the pathogen, and often in conflict with each other via trade-offs. Transmission modes may vary among pathogen strains and among host populations. Evolutionary changes in transmission mode have been inferred through experimental and phylogenetic studies, including changes in transmission associated with host shifts and with evolution of the unusually complex life cycles of many parasites. Understanding the forces that determine the evolution of particular transmission modes presents a fascinating medley of problems for which there is a lack of good data and often a lack of conceptual understanding or appropriate methodologies. Our best information comes from studies that have been focused on the vertical versus horizontal transmission dichotomy. With other kinds of transitions, theoretical approaches combining epidemiology and population genetics are providing guidelines for determining when and how rapidly new transmission modes may evolve, but these are still in need of empirical investigation and application to particular cases. Obtaining such knowledge is a matter of urgency in relation to extant disease threats.This article is part of the themed issue 'Opening the black box: re-examining the ecology and evolution of parasite transmission'.


Subject(s)
Animal Diseases/transmission , Biological Evolution , Host-Parasite Interactions , Animals , Host-Pathogen Interactions
3.
Philos Trans R Soc Lond B Biol Sci ; 372(1719)2017 May 05.
Article in English | MEDLINE | ID: mdl-28289261

ABSTRACT

The harm that pathogens cause to hosts during infection, termed virulence, varies across species from negligible to a high likelihood of rapid death. Classic theory for the evolution of virulence is based on a trade-off between pathogen growth, transmission and host survival, which predicts that higher within-host growth causes increased transmission and higher virulence. However, using data from 61 human pathogens, we found the opposite correlation to the expected positive correlation between pathogen growth rate and virulence. We found that (i) slower growing pathogens are significantly more virulent than faster growing pathogens, (ii) inhaled pathogens and pathogens that infect via skin wounds are significantly more virulent than pathogens that are ingested, but (iii) there is no correlation between symptoms of infection that aid transmission (such as diarrhoea and coughing) and virulence. Overall, our results emphasize how virulence can be influenced by mechanistic life-history details, especially transmission mode, that determine how parasites infect and exploit their hosts.This article is part of the themed issue 'Opening the black box: re-examining the ecology and evolution of parasite transmission'.


Subject(s)
Biological Evolution , Disease Transmission, Infectious , Host-Parasite Interactions , Parasites/physiology , Parasites/pathogenicity , Animals , Humans , Life History Traits , Parasites/growth & development , Virulence
4.
Philos Trans R Soc Lond B Biol Sci ; 372(1719)2017 May 05.
Article in English | MEDLINE | ID: mdl-28289263

ABSTRACT

It is becoming increasingly clear that the evolution of infectious disease is influenced by host population structure. Theory predicts that parasites should be more 'prudent'-less transmissible-in spatially structured host populations. However, here we (i) highlight how low transmission, the phenotype being selected for in this in context, may also be achieved by rapacious host exploitation, if fast host exploitation confers a local, within-host competitive advantage and (ii) test this novel concept in a bacteria-virus system. We found that limited host availability and, to a lesser extent, low relatedness favour faster-killing parasites with reduced transmission. By contrast, high host availability and high relatedness favour slower-killing, more transmissible parasites. Our results suggest high, rather than low, virulence may be selected in spatially structured host-parasite communities where local competition and hence selection for a within-host fitness advantage is high.This article is part of the themed issue 'Opening the black box: re-examining the ecology and evolution of parasite transmission'.


Subject(s)
Bacteria/virology , Bacteriophages/physiology , Biological Evolution , Host-Pathogen Interactions , Animals , Bacteriophages/pathogenicity , Models, Biological , Virulence
5.
Philos Trans R Soc Lond B Biol Sci ; 369(1642): 20130365, 2014 May 19.
Article in English | MEDLINE | ID: mdl-24686936

ABSTRACT

One of the most striking facts about parasites and microbial pathogens that has emerged in the fields of social evolution and disease ecology in the past few decades is that these simple organisms have complex social lives, indulging in a variety of cooperative, communicative and coordinated behaviours. These organisms have provided elegant experimental tests of the importance of relatedness, kin discrimination, cooperation and competition, in driving the evolution of social strategies. Here, we briefly review the social behaviours of parasites and microbial pathogens, including their contributions to virulence, and outline how inclusive fitness theory has helped to explain their evolution. We then take a mechanistically inspired 'bottom-up' approach, discussing how key aspects of the ways in which parasites and pathogens exploit hosts, namely public goods, mobile elements, phenotypic plasticity, spatial structure and multi-species interactions, contribute to the emergent properties of virulence and transmission. We argue that unravelling the complexities of within-host ecology is interesting in its own right, and also needs to be better incorporated into theoretical evolution studies if social behaviours are to be understood and used to control the spread and severity of infectious diseases.


Subject(s)
Biological Evolution , Genetic Fitness , Host-Pathogen Interactions , Infections/physiopathology , Microbial Interactions/genetics , Models, Biological , Social Behavior , Phenotype , Virulence/genetics
6.
Trends Ecol Evol ; 28(10): 592-6, 2013 Oct.
Article in English | MEDLINE | ID: mdl-23968968

ABSTRACT

The evolution of parasite-imposed host harm (virulence) will be affected by numerous factors, not least the range of hosts that parasites can infect. Here, we consider four ways that parasite host range (generalism) might directly affect observed levels of parasite virulence: costs of generalism, multiplicity of infection, maladaptive virulence, and host availability. Integrating parasite infectivity range with life-history evolution will generate novel general hypotheses for the evolutionary ecology of virulence, as well as explicit predictions about the virulence of emerging diseases resulting from host shifts.


Subject(s)
Biological Evolution , Parasites/pathogenicity , Parasitic Diseases/transmission , Animals , Parasitic Diseases/microbiology , Parasitic Diseases/parasitology , Virulence
7.
Curr Biol ; 23(2): 139-42, 2013 Jan 21.
Article in English | MEDLINE | ID: mdl-23246405

ABSTRACT

Coinfection of parasite genotypes can select for various changes in parasite life history strategies relative to single genotype infections, with consequences for disease dynamics and severity. However, even where coinfection is common, a parasite genotype is also likely to regularly experience single genotype infections over relatively short periods of evolutionary time, due to chance, changes in local disease transmission, and parasite population structuring. Such alternating conditions between single genotype and coinfections will impose conflicting pressures on parasites, potentially selecting for facultative responses to coinfection. Although such adaptive phenotypic plasticity in response to social environment has been observed in protozoan parasites and viruses, here we show it evolving in real time in response to coinfection under conditions in which both single infections and coinfections are common. We experimentally evolved an obligate-killing virus under conditions of single virus infections (single lines) or a mix of single infections and coinfections (mixed lines) and found mixed lines to evolve a plastic lysis time: they killed host cells more rapidly when coinfecting than when infecting alone. This behavior resulted in high fitness under both infection conditions. Such plasticity has important consequences for the epidemiology of infectious diseases and the evolution of cooperation.


Subject(s)
Adaptation, Biological , Bacteriophages/genetics , Biological Evolution , Phenotype , Pseudomonas fluorescens/virology , Coinfection
8.
Biol Lett ; 8(5): 768-71, 2012 Oct 23.
Article in English | MEDLINE | ID: mdl-22628097

ABSTRACT

An influential ecological theory, the intermediate disturbance hypothesis (IDH), predicts that intermediate levels of disturbance will maximize species diversity. Empirical studies, however, have described a wide variety of diversity-disturbance relationships (DDRs). Using experimental populations of microbes, we show that the form of the DDR depends on an interaction between disturbance frequency and intensity. We find that diversity shows a monotonically increasing, unimodal or flat relationship with disturbance, depending on the values of the disturbance aspects considered. These results confirm recent theoretical predictions, and potentially reconcile the conflicting body of empirical evidence on DDRs.


Subject(s)
Biodiversity , Ecology/methods , Pseudomonas fluorescens/physiology , Biofilms , Ecosystem , Environment , Models, Biological , Models, Statistical , Models, Theoretical , Population Dynamics , Pseudomonas fluorescens/metabolism
9.
PLoS Pathog ; 8(2): e1002512, 2012 Feb.
Article in English | MEDLINE | ID: mdl-22359500

ABSTRACT

The number of pathogens that are required to infect a host, termed infective dose, varies dramatically across pathogen species. It has recently been predicted that infective dose will depend upon the mode of action of the molecules that pathogens use to facilitate their infection. Specifically, pathogens which use locally acting molecules will require a lower infective dose than pathogens that use distantly acting molecules. Furthermore, it has also been predicted that pathogens with distantly acting immune modulators may be more virulent because they have a large number of cells in the inoculums, which will cause more harm to host cells. We formally test these predictions for the first time using data on 43 different human pathogens from a range of taxonomic groups with diverse life-histories. We found that pathogens using local action do have lower infective doses, but are not less virulent than those using distant action. Instead, we found that virulence was negatively correlated with infective dose, and higher in pathogens infecting wounded skin, compared with those ingested or inhaled. More generally, our results show that broad-scale comparative analyses can explain variation in parasite traits such as infective dose and virulence, whilst highlighting the importance of mechanistic details.


Subject(s)
Bacteria/pathogenicity , Fungi/pathogenicity , Virulence/physiology , Viruses/pathogenicity , Humans , Parasitic Diseases/mortality
10.
Proc Biol Sci ; 279(1732): 1405-11, 2012 Apr 07.
Article in English | MEDLINE | ID: mdl-21993501

ABSTRACT

Empirical data suggest that low levels of promiscuity have played a key role in the evolution of cooperative breeding and eusociality. However, from a theoretical perspective, low levels of promiscuity can favour dispersal away from the natal patch, and have been argued to select against cooperation in a way that cannot be explained by inclusive fitness theory. Here, we use an inclusive fitness approach to model selection to stay and help in a simple patch-structured population, with strict density dependence, where helping increases the survival of the breeder on the patch. Our model predicts that the level of promiscuity has either no influence or a slightly positive influence on selection for helping. This prediction is driven by the fact that, in our model, staying to help leads to increased competition between relatives for the breeding position-when promiscuity is low (and relatedness is high), the best way to aid relatives is by dispersing to avoid competing with them. Furthermore, we found the same results with an individual-based simulation, showing that this is not an area where inclusive fitness theory 'gets it wrong'. We suggest that our predicted influence of promiscuity is sensitive to biological assumptions, and that if a possibly more biologically relevant scenario were examined, where helping provided fecundity benefits and there was not strict density dependence, then low levels of promiscuity would favour helping, as has been observed empirically.


Subject(s)
Biological Evolution , Sexual Behavior, Animal , Animals , Breeding , Cooperative Behavior , Female , Genetic Fitness , Male , Models, Biological , Social Behavior
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