Virulence and competitive ability in genetically diverse malaria infections - PubMed (original) (raw)

Comparative Study

. 2005 May 24;102(21):7624-8.

doi: 10.1073/pnas.0500078102. Epub 2005 May 13.

Affiliations

Comparative Study

Virulence and competitive ability in genetically diverse malaria infections

Jacobus C de Roode et al. Proc Natl Acad Sci U S A. 2005.

Abstract

Explaining parasite virulence is a great challenge for evolutionary biology. Intuitively, parasites that depend on their hosts for their survival should be benign to their hosts, yet many parasites cause harm. One explanation for this is that within-host competition favors virulence, with more virulent strains having a competitive advantage in genetically diverse infections. This idea, which is well supported in theory, remains untested empirically. Here we provide evidence that within-host competition does indeed select for high parasite virulence. We examine the rodent malaria Plasmodium chabaudi in laboratory mice, a parasite-host system in which virulence can be easily monitored and competing strains quantified by using strain-specific real-time PCR. As predicted, we found a strong relationship between parasite virulence and competitive ability, so that more virulent strains have a competitive advantage in mixed-strain infections. In transmission experiments, we found that the strain composition of the parasite populations in mosquitoes was directly correlated with the composition of the blood-stage parasite population. Thus, the outcome of within-host competition determined relative transmission success. Our results imply that within-host competition is a major factor driving the evolution of virulence and can explain why many parasites harm their hosts.

PubMed Disclaimer

Figures

Fig. 1.

Fig. 1.

Parasite densities over time (mean ± 1 SEM) for AS3a, AS3m, and AS3v. Graphs compare AS with AJ strains in mixed infections (A–C), AS strains in mixed and single infections (D–F), and AJ strains in mixed and single infections (G–I). AS strains persisted for at least 30 days when infecting mice alone but for a much shorter time period in competition with AJ [F(1,24) = 42, P < 0.001 for AS3a, AS3m, and AS3v; F(1,61) = 36, P < 0.001 for all AS strains]. The limit of detection was 100 parasites per microliter of blood, so that y axes start at 2.

Fig. 2.

Fig. 2.

AS and AJ parasite densities in single and mixed infections (mean ± 1 SEM). Strains of both lineages were suppressed by the presence of a competitor.

Fig. 3.

Fig. 3.

The relationships between virulence and competitiveness (A) and virulence and competitive suppression (B). Virulence of the AS strains was measured as the anemia induced in single-strain infections and expressed as the fraction of the anemia contemporaneously induced by single-strain infections of AJ. (A) Competitiveness was defined as the proportion that AS obtained of the total parasite population in the mixed-strain infections. Regression analysis was done by using arcsine-square-root-transformed data; the plotted regression line is back-transformed. Because the minimal model included a quadratic virulence term (P = 0.035, _R_2 = 0.90), the relationship between virulence and competitiveness is curvilinear. (B) Relative competitive suppression was defined as the proportional reduction of parasite numbers of AS strains in competition from what they achieved in single-strain infections. Regression analysis was done by using arcsine-square-root-transformed data (P = 0.021, _R_2 = 0.63); the plotted regression line is back-transformed.

Fig. 4.

Fig. 4.

Transmission of AS to mosquitoes. (A) Proportions of mosquitoes infected with AS parasites from single and mixed infections. (B) Numbers of AS parasites per infected mosquito from single and mixed infections. For A and B, the same patterns were found for both experiments (single/mixed × experiment interaction; P > 0.05). (C) Proportion of AS (calculated by summing the number of AS parasites over all mosquitoes fed on a single mouse divided by the overall AS+AJ parasites in those mosquitoes) vs. its asexual proportion in the mouse [F(1,15) = 7.04, P = 0.018, _R_2 = 0.27]. (D) Average proportion of AS (calculated by determining the proportion of AS in each PCR-positive mosquito and then averaging these per mouse) vs. its asexual proportion in the mouse [F(1,15) = 9.54, P = 0.007, _R_2 = 0.35]. For C and D, the same patterns were found in both experiments (experiment and blood-stage proportion AS × experiment interaction: P > 0.05).

References

    1. Zimmer, C. (2001) Parasite Rex: Inside the Bizarre World of Nature's Most Dangerous Creatures (Simon & Schuster, New York).
    1. Anderson, R. M. & May, R. M. (1982) Parasitology 85**,** 411–426. -PubMed
    1. Ebert, D. (1999) in Evolution in Health and Disease, ed. Stearns, S. C. (Oxford Univ. Press, Oxford), pp. 161–172.
    1. Levin, B. R. (1996) Emerg. Infect. Dis. 2**,** 93–102. -PMC -PubMed
    1. Ebert, D. (1998) Science 282**,** 1432–1435. -PubMed

Publication types

MeSH terms

LinkOut - more resources