The evolution and genetics of virus host shifts

Abstract

Emerging viral diseases are often the product of a host shift, where a pathogen jumps from its original host into a novel species. Phylogenetic studies show that host shifts are a frequent event in the evolution of most pathogens, but why pathogens successfully jump between some host species but not others is only just becoming clear. The susceptibility of potential new hosts can vary enormously, with close relatives of the natural host typically being the most susceptible. Often, pathogens must adapt to successfully infect a novel host, for example by evolving to use different cell surface receptors, to escape the immune response, or to ensure they are transmitted by the new host. In viruses there are often limited molecular solutions to achieve this, and the same sequence changes are often seen each time a virus infects a particular host. These changes may come at a cost to other aspects of the pathogen's fitness, and this may sometimes prevent host shifts from occurring. Here we examine how these evolutionary factors affect patterns of host shifts and disease emergence.

Figure 1. Two ways in which host relatedness may effect a pathogen's ability to host shift.

The bars at the tips of the trees show a measure of pathogen infection success, with the bar in red representing the pathogen's natural host species. (A) The pathogen is less successful in host clades more distantly related to its natural host. (B) “Patches” of highly susceptible—or highly resistant—clades of hosts, may be scattered across the host phylogeny independently from their distance from the natural host. All of the species in the clade labelled “a” are equally distantly related from the pathogen's natural host. However, the species in the clade marked “b” are highly susceptible, despite being distantly related to the natural host.

Figure 2. Examples of parallel adaptations following host shifts.

(A) Parallel genetic changes in five replicate lines of Hibiscus chlorotic ring spot virus. The white boxes represent the viral genome, and the coloured blocks represent mutations. The virus naturally infects Hibiscus plants, but following five passages in an alternate host, (Chenopodium quinoa) the same eight mutations repeatedly occur . (B) Parallel genetic changes in codon 30 of the gag gene (Met to Arg) following three independent transfers of SIVcpz into humans . When a chimp was subsequently infected with HIV-1, the residue reverted back to Met. The coloured blocks represent either a Met (yellow) or Arg (blue) at codon position 30 in the HIV gag gene. (C) Parallel changes in protein function following independent transfers of SIVs from chimpanzees (HIV-1) and sooty mangabeys (HIV-2) into humans. SIV Nef protein does not antagonise tetherin in humans, and so other HIV proteins have evolved the ability to antagonise tetherin . The exception to this is HIV-1 group O viruses, which do not appear to have evolved anti-tetherin activity. In HIV-1 group N viruses the evolution of anti-tetherin activity in Vpu may have come at a cost, as Vpu no longer degrades CD4 receptors to aid the release of viral particles . The coloured gene names in the schematic represent the gene that provides the anti-tetherin function in that host and viral lineage.

Figure 3. Examples of how patterns of host shifts can affect the distribution of pathogens across the host phylogeny.

Each column shows the presence of a different pathogen, with a coloured circle representing the presence of that pathogen. In panel A, pathogens preferentially shift between closely related hosts, while in B closely related host species have similar levels of susceptibility to infection, regardless of the source of the pathogen (with two increases in host resistance occurring at the asterisks on the host phylogeny). Both processes result in closely related host species harbouring similar pathogens, and in some host clades harbouring more pathogen species. However, in A, but not B, host species with more close relatives tend to have more pathogens. For example, the phylogenetically isolated species at the bottom of the tree is not infected by any of the three pathogens in A, but is in B.