Biological Reviews



Review Article

Pathogen survival in the external environment and the evolution of virulence


Bruno A. Walther a1a2a3c1 and Paul W. Ewald a1
a1 Department of Biology, Amherst College, Amherst, MA 01002-2237, USA
a2 Department of Zoology, Oxford University, Oxford, OX1 3PS, UK
a3 Zoological Museum, University of Copenhagen, Universitetsparken 15, 2100 København Ø, Denmark

Article author query
walther ba   [PubMed][Google Scholar] 
ewald pw   [PubMed][Google Scholar] 

Abstract

Recent studies have provided evolutionary explanations for much of the variation in mortality among human infectious diseases. One gap in this knowledge concerns respiratory tract pathogens transmitted from person to person by direct contact or through environmental contamination. The sit-and-wait hypothesis predicts that virulence should be positively correlated with durability in the external environment because high durability reduces the dependence of transmission on host mobility. Reviewing the epidemiological and medical literature, we confirm this prediction for respiratory tract pathogens of humans. Our results clearly distinguish a high-virulence high-survival group of variola (smallpox) virus, Mycobacterium tuberculosis, Corynebacterium diphtheriae, Bordetella pertussis, Streptococcus pneumoniae, and influenza virus (where all pathogens have a mean percent mortality [gt-or-equal, slanted]0.01% and mean survival time >10 days) from a low-virulence low-survival group containing ten other pathogens. The correlation between virulence and durability explains three to four times of magnitude of difference in mean percent mortality and mean survival time, using both across-species and phylogenetically controlled analyses. Our findings bear on several areas of active research and public health policy: (1) many pathogens used in the biological control of insects are potential sit-and-wait pathogens as they combine three attributes that are advantageous for pest control: high virulence, long durability after application, and host specificity; (2) emerging pathogens such as the ‘hospital superbug’ methicillin-resistant Staphylococcus aureus (MRSA) and potential bioweapons pathogens such as smallpox virus and anthrax that are particularly dangerous can be discerned by quantifying their durability; (3) hospital settings and the AIDS pandemic may provide footholds for emerging sit-and-wait pathogens; and (4) studies on food-borne and insect pathogens point to future research considering the potential evolutionary trade-offs and genetic linkages between virulence and durability.

(Published Online November 8 2004)
(Received August 27 2003)
(Revised March 15 2004)
(Accepted March 22 2004)


Key Words: virulence; durability; mortality; transmission; sit-and-wait pathogens; evolution; infectious disease.

Correspondence:
c1 Zoologisk Museum, Kobenhavns Universitet, Universitetsparken 15, DK 2100 Kobenhavn Ø, Denmark. Tel: +45-3532-1051. Fax: +45-3532-1010. E-mail: reprints@bruno-walther.de