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  • Review Article
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Humans and evolutionary and ecological forces shaped the phylogeography of recently emerged diseases

Nature Reviews Microbiology volume 7, pages 813–821 (2009)Cite this article

Key Points

  • The movement of humans and commerce facilitate the emergence of new infectious diseases. Local pathogen populations can take advantage of human activities to create pandemics.

  • Recently emerged pathogens are very homogeneous owing to their recent derivation from another species or group. Even among highly similar subtypes, just a subset of strains becomes globally distributed owing to their high fitness.

  • Bacillus anthracis (which causes anthrax) spread globally owing to spore contamination of animal products such as hair, hides and bones. Long-range transmission of anthrax does not occur naturally but rather depends on humans.

  • Yersinia pestis (which causes plague) evolved in Asia and was spread globally by human-mediated movement of infected rodents and their fleas. Regional and local ecological establishment is not uniform and is highly dependent on the make-up of local rodent populations.

  • Francisella tularensis (which causes tularaemia) has four subspecies, each with distinctive geographical distributions. Only F. tularensis subsp. holarctica is commonly found on multiple continents and represents a highly fit genotype that has clonally expanded in a circumpolar fashion.

  • Local pathogen populations may evolve 'hopeful monster' subtypes that can take advantage of ecological opportunities. In several cases, this opportunity has been human-mediated, long-distance dispersal with severe consequences for humans.

Abstract

The development of human civilizations and global commerce has led to the emergence and worldwide circulation of many infectious diseases. Anthrax, plague and tularaemia are three zoonotic diseases that have been intensely studied through genome characterization of the causative species and phylogeographical analyses. A few highly fit genotypes in each species represent the causative agents for most of the observed disease cases. Together, mutational and selective forces create highly adapted pathogens, but this must be coupled with ecological opportunities for global expansion. This Review describes the distributions of the bacteria that cause anthrax, plague and tularaemia and investigates the forces that created clonal structures in these species.

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Figure 1: Infection cycles of Bacillus anthracis, Yersinia pestis Francisella tularensis.
Figure 2: Phylogeography of Bacillus anthracis.
Figure 3: Phylogeography of Yersinia pestis.
Figure 4: Phylogeography of Francisella tularensis.

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Acknowledgements

We are grateful to J. Foster, R. Okinaka and T. Pearson for their comments. This work was supported by the US National Institutes of Health (GM060795, AI070183), the Pacific-Southwest Region Center of Excellence (AI065359) and the Department of Homeland Security Science and Technology Directorate (NBCH2070001 and HSHQDC-08-C00158).

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Authors and Affiliations

  1. The Center for Microbial Genetics and Genomics, Northern Arizona University, Flagstaff, 86011-4073, Arizona, USA

    Paul S. Keim

  2. Pathogen Genomics Division, The Translational Genomics Research Institute, 3051 West Shamrell Boulevard, Suite 106, Flagstaff, 86001, Arizona, USA

    David M. Wagner

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Correspondence to Paul S. Keim.

Related links

Glossary

Mutation rate

The frequency with which nucleotide changes occur in a genome, usually standardized by events per generation.

Horizontal gene transfer

The movement of DNA from the genome of one organism into that of another; also known as lateral gene transfer. The three primary mechanisms are transformation, which involves uptake of naked DNA from the environment by a bacterium, transduction, in which phages transfer DNA between organisms, and conjugation, which involves the transfer of DNA directly from bacterium to bacterium.

Neutral genetic variation

Polymorphic genetic features that have no impact on the survival or reproductive success of the organism.

Fixation

A genetic phenomenon in which a previously polymorphic feature takes on the same state in every individual in a population and, hence, is no longer polymorphic.

Clonal organism

An organism that reproduces only by the division of somatic cells, without gene transfer or recombination. In this situation, genetic diversity is generated by mutation alone and not by gene transfer or recombination.

Recently emerged pathogen

A pathogen species, subspecies, population or genotype with a short evolutionary history. It emerges from another species or population, possibly owing to a mutation that increases its fitness and leads to an increase in its frequency and distribution. The recent emergence of such pathogens is often inferred from the fact that there is little genetic diversity among individual isolates.

Host shifting

Acquiring the capacity to infect a new host species and perhaps becoming adapted specifically to that new host.

Phylogeography

Combining phylogenetics and geography to understand the geographical distribution of evolutionary patterns in a given organism.

Phylogenetically informative characters

Polymorphic features (for example, a locus with multiple alleles) that have a genotype (for example, an allele) shared by two or more members (for example, isolates or strains) of the study group (for example, a population or a species), providing insights into the evolutionary relationships among members.

Homoplasy

The occurrence of the same genotype in two organisms that is due not to shared descent but rather to other forces, such as a reverse mutation or recombination.

Pleiotropic mutation

A single genetic change that leads to multiple phenotypes; for example, a regulatory mutation may affect many different genes and, therefore, the multiple phenotypes associated with those different genes.

Obligate pathogen

An organism that can only survive in a host or vector and cannot persist directly in the environment.

Sylvatic

Pertaining to wild animals as opposed to commensal animals, which are associated with humans.

Phylogeny

A model of the evolutionary history of a set of individuals, species or other taxonomic units. Phylogenies are hypotheses that are based on the analysis of phylogenetically informative characters that arose as the organisms evolved. They are traditionally used to understand the evolution of species and other taxonomic units but are applicable to clonally propagating populations as well.

Opportunistic pathogen

An organism that is normally benign but, given the right situation (for example, an immunocompromised host), can cause disease. Often humans or other hosts that are occasionally infected by these organisms are not important to the overall lifestyle of these pathogens and are dead-end hosts.

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Keim, P., Wagner, D. Humans and evolutionary and ecological forces shaped the phylogeography of recently emerged diseases. Nat Rev Microbiol 7, 813–821 (2009). https://doi.org/10.1038/nrmicro2219

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