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Review
. 2013 Feb;8(2):155-76.
doi: 10.2217/fmb.12.139.

Factors shaping the adaptive landscape for arboviruses: implications for the emergence of disease

Lark L Coffey  1 , Naomi Forrester, Konstantin Tsetsarkin, Nikos Vasilakis, Scott C Weaver
Affiliations
Review

Factors shaping the adaptive landscape for arboviruses: implications for the emergence of disease

Lark L Coffey et al. Future Microbiol. 2013 Feb.

Abstract

Many examples of the emergence or re-emergence of infectious diseases involve the adaptation of zoonotic viruses to new amplification hosts or to humans themselves. These include several instances of simple mutational adaptations, often to hosts closely related to the natural reservoirs. However, based on theoretical grounds, arthropod-borne viruses, or arboviruses, may face several challenges for adaptation to new hosts. Here, we review recent findings regarding adaptive evolution of arboviruses and its impact on disease emergence. We focus on the zoonotic alphaviruses Venezuelan equine encephalitis and chikungunya viruses, which have undergone adaptive evolution that mediated recent outbreaks of disease, as well as the flaviviruses dengue and West Nile viruses, which have emerged via less dramatic adaptive mechanisms.

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Figures

Figure 1
Figure 1. Fitness landscapes for arboviruses
(A) Theoretical, 3D landscape for infection of the vertebrate host; (B) theoretical, 3D landscape for infection of the vector; (C) superimposition of vertebrate and vector landscapes, demonstrating limited genotypes that are highly fit in both hosts (overlapping peaks). Peaks with partial overlap (arrows) could result in subtle shifts in the mutant swarm as an arbovirus alternates between vertebrate and vector infections. (D) Fitness landscape for CHIKV transmission by the epidemic mosquito vector, Aedes albopictus. The three envelope glycoprotein amino acids with major effects on A. albopictus infection are indicated, demonstrating sequential adaptive envelope glycoprotein substitutions in the IOL and epistatic limitations in the Asian lineage. The E2-L210Q mutation observed in India in 2009 is a second-step mutation that increases infectivity and dissemination. The Asian genotype needs one additional substitution in the E1 protein (T98A) compared with the IOL for the major fitness of the E1-A226V substitution to be manifested. This epistatic interaction apparently has prevented the Asian lineage from adapting to A. albopictus for the past six decades. Green lettering indicates ancestral residues; red lettering indicates derived residues associated with adaptation to A. albopictus. CHIKV: Chikungunya virus; IOL: Indian Ocean lineage. Adapted with permission from [108].
Figure 2
Figure 2. Arbovirus transmission cycles showing ancestral enzootic cycles, epizootic cycles involving amplification by domesticated animals, such as horses, and endemic/epidemic cycles in urban habitats involving human amplification hosts
CHIKV: Chikungunya virus; DENV: Dengue virus; VEEV: Venezuelan equine encephalitis virus; WNV: West Nile virus.
Figure 3
Figure 3. Virion morphology and genome organization for alphaviruses and flaviviruses
CAP: Capsid; E: Envelope; prM: Premembrane. Adapted with permission from [–112].
Figure 4
Figure 4. Evolutionary history of Chikungunya virus emergence
(A) Recent history of CHIKV outbreaks and (B) phylogenetic relationships of CHIKV genotypes. The phylogenetic tree for 26 representative CHIKV strains was constructed using the maximum likelihood method. Amino acid residues at positions E1-226 and E1-98 are indicated. CHIKV: Chikungunya virus; ECSA: East-central-south-African; IOL: Indian Ocean lineage; WA: West Africa. Adapted with permission from [24].
Figure 5
Figure 5. Emergence of urban dengue virus transmission cycles and lineages from sylvatic progenitors
DENV: Dengue virus.
Figure 6
Figure 6. Route of infection and potential bottlenecks during arbovirus infection of a mosquito
The route of virus dissemination from an infectious blood meal is shown by solid boxes, and the anatomical placement of each stage is designated by the letters (A–F) on the mosquito. The potential bottlenecks associated with physical barriers that the virus encounters during dissemination are shown in dashed boxes. Adapted with permission from [113].
Figure 7
Figure 7. Arbovirus population dynamics in vector infection
Lines represent individual arbovirus genomes; colored dots show mutations. The average sequence (consensus) in each population is shown, and is often unchanged during infection. Studies with West Nile virus, Venezuelan equine encephalitis virus and Chikungunya virus show that the composition of the mutant spectrum changes as viruses traverse anatomical barriers and experience genetic bottlenecks (diminishing slope showing decreased population size), including during infection and escape from the midgut epithelium, but that replication in secondary tissues regenerates genetic diversity (increasing slope) at levels comparable to populations ingested from the vertebrate host. In some cases, compartmentalization of individual variants (e.g., purple transmitted mutation) occurs in selected tissues, and some mutations (e.g., green) arise de novo in secondary tissues. In general, these studies show that arboviruses can circumvent anatomical barriers that produce genetic bottlenecks in mosquitoes, such that the size of the mutant spectrum that disseminates and is transmitted by vectors is not significantly reduced.
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