Specific and nonspecific host adaptation during arboviral experimental evolution

Abstract

During the past decade or so, there has been a substantial body of work to dissect arboviral evolution and to develop models of adaptation during host switching. Regardless of what species serve as host or vectors, and of the geographic distribution and the mechanisms of replication, arboviruses tend to have slow evolutionary rates in nature. The hypothesis that this is the result of replication in the disparate environments provided by host and vector did not receive solid experimental support in any of the many viral species tested. Instead, it seems that from the virus's point of view, either the two environments are sufficiently similar or one of the environments so dominates viral evolution that there is tolerance for suboptimal adaptation to the other environment. Replication in alternating environments has an unexpected cost in that there is decreased genetic variance that translates into a compromised adaptability for bypassed environments. Arboviruses under strong and continuous positive selection may have unusual patterns of genomic changes, with few or no mutations accumulated in the consensus sequence or with dN/dS values typically consistent with random drift in DNA-based organisms.

Fig. 1

Fitness landscapes showing differences in robustness. Two peaks are represented: a flat peak on the left and a sharp peak on the right. Black diamonds represent progenitors that start to replicate and generate the progeny represented by grey diamonds. At high mutation rates, the progeny will be displaced from the site where the progenitor sits. If the peak is flat (high robustness), fitness is maintained; but if the peak is sharp, there is fitness loss (low robustness) and the populations will be outcompeted.

Fig. 2

Consensus sequence and population diversity. Lines represent genomes and circles indicate mutations. For simplicity, we ignore beneficial variation; grey circles represent neutral mutations and white circles indicate deleterious mutations. The consensus represents the average sequence at each locus and is shown at the bottom. The consensus sequence of a viral progenitor (a) may remain unchanged despite substantial - and biologically significant - increase (b) or decrease (c) in population heterogeneity.

Fig. 3

Natural cycles of arboviruses. Different species have one or more of the steps presented in this figure. Human infections are typically the result of transmission during urban cycles or spillover from natural, sylvatic cycles.

Fig. 4

Fitness landscape during host switch. Solid lines and dotted lines represent the landscapes provided by two different environments. The original proposal (a) was that vector and host (or different hosts) provide landscapes with only a few and minor overlapping peaks where the virus could survive in both environments (indicated by the arrow). Experimental results indicate that this is not the case and, instead, in some cases there are multiple or major peaks (arrows in b) or one of the environments - typically the vector - dominates the evolution of the virus, which climbs fitness peaks in such environment (indicated by asterisks in c) even though these correspond to fitness valleys in the other environment.