Association and Host Selectivity in Multi-Host Pathogens

PLOS ONE, Dec 2006

The distribution of multi-host pathogens over their host range conditions their population dynamics and structure. Also, host co-infection by different pathogens may have important consequences for the evolution of hosts and pathogens, and host-pathogen co-evolution. Hence it is of interest to know if the distribution of pathogens over their host range is random, or if there are associations between hosts and pathogens, or between pathogens sharing a host. To analyse these issues we propose indices for the observed patterns of host infection by pathogens, and for the observed patterns of co-infection, and tests to analyse if these patterns conform to randomness or reflect associations. Applying these tests to the prevalence of five plant viruses on 21 wild plant species evidenced host-virus associations: most hosts and viruses were selective for viruses and hosts, respectively. Interestingly, the more host-selective viruses were the more prevalent ones, suggesting that host specialisation is a successful strategy for multi-host pathogens. Analyses also showed that viruses tended to associate positively in co-infected hosts. The developed indices and tests provide the tools to analyse how strong and common are these associations among different groups of pathogens, which will help to understand and model the population biology of multi-host pathogens.

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Association and Host Selectivity in Multi-Host Pathogens

Citation: Malpica JM, Sacristan S, Fraile A, Garca-Arenal F ( Association and Host Selectivity in Multi-Host Pathogens Jose M. Malpica 0 1 2 Soledad Sacrista n 0 1 2 Aurora Fraile 0 1 2 Fernando Garca-Arenal 0 1 2 0 Funding: This work was in part supported by grant AGL2004-03496, Ministerio de Educacio n y Ciencia, Spain, to AF. SS was in receipt of a FPU fellowship , Ministerio de Educacio n y Ciencia , Spain 1 Academic Editor: Angus Buckling, Oxford University , United Kingdom 2 1 Departamento de Biotecnolog a, Instituto Nacional de Investigaci o n Agraria y Alimentaria , Madrid , Spain , 2 Departamento de Biotecnolog a y Centro de Biotecnolog a y Gen o mica de Plantas, Universidad Polit e cnica de Madrid , Madrid , Spain The distribution of multi-host pathogens over their host range conditions their population dynamics and structure. Also, host co-infection by different pathogens may have important consequences for the evolution of hosts and pathogens, and hostpathogen co-evolution. Hence it is of interest to know if the distribution of pathogens over their host range is random, or if there are associations between hosts and pathogens, or between pathogens sharing a host. To analyse these issues we propose indices for the observed patterns of host infection by pathogens, and for the observed patterns of co-infection, and tests to analyse if these patterns conform to randomness or reflect associations. Applying these tests to the prevalence of five plant viruses on 21 wild plant species evidenced host-virus associations: most hosts and viruses were selective for viruses and hosts, respectively. Interestingly, the more host-selective viruses were the more prevalent ones, suggesting that host specialisation is a successful strategy for multi-host pathogens. Analyses also showed that viruses tended to associate positively in co-infected hosts. The developed indices and tests provide the tools to analyse how strong and common are these associations among different groups of pathogens, which will help to understand and model the population biology of multihost pathogens. - INTRODUCTION Pathogens have highly variable host ranges: in natural conditions some infect only one or a few related species (i.e., specialist pathogens) while other can infect a wide range of hosts belonging to different taxonomic groups (i.e., multi-host or generalist pathogens). A large fraction of described pathogens of humans, animals and plants are generalists [13]. The ability to infect different hosts conditions the epidemiology and pathogenicity of generalist pathogens and, therefore, is highly relevant for pathogen management and disease control [1,4]. The distribution of multihost pathogens over their host range, i.e. the frequency of infection in the various host species within an ecosystem, may vary largely, which could determine the population dynamics and structure of the pathogen. The distribution of a pathogen species over its host range may also determine important aspects of its biology in hosts significant from an anthropocentric viewpoint (i.e. target hosts), such as reservoirs and inoculum sources, emergence and reemergence, population thresholds for disease invasion or critical community size for disease persistence [e.g., 1,47]. Animal or plant species may be hosts for a range of pathogens, and most host populations encounter a large number of different pathogen species [8]. For significant host species, there is abundant evidence of differences in the infection frequency of the various pathogen species present in an ecosystem. The distribution of pathogens over their hosts, and the distribution of different pathogens within a host species, will affect the frequency of multiple infection of an individual host by different pathogens. Multiple infection may have important consequences for the infected hosts, for the pathogens, and for host-pathogen coevolution [8,9]. In the host, frequent co-infections may lead to heterozygote superiority against multiple pathogens and contribute to the persistence in host populations of alleles conferring susceptibility to disease [10]. In multiple infected hosts, pathogens can cooperate or can compete for host resources, which will affect each others fitness. Hence, multiple infections will be a factor in pathogen evolution. Theoretical analyses predict that the withinhost dynamics of microparasites in multiple infected hosts may have important consequences in the evolution of their virulence [1114], and there is evidence that multiple infection may result in either increased or reduced virulence [e.g., 1517]. Multiple infection of a host may also directly affect the genetic diversity of the pathogen population, as co-infection is a prerequisite for genetic exchange between different pathogen species or strains. Also, infection by one pathogen may result in an increased host susceptibility to a second pathogen, a common phenomenon named facilitation or predisposition by animal (...truncated)


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José M. Malpica, Soledad Sacristán, Aurora Fraile, Fernando García-Arenal. Association and Host Selectivity in Multi-Host Pathogens, PLOS ONE, 2006, 1, DOI: 10.1371/journal.pone.0000041