Parallel molecular evolution and adaptation in viruses

Abstract

Parallel molecular evolution is the independent evolution of the same genotype or phenotype from distinct ancestors. The simple genomes and rapid evolution of many viruses mean they are useful model systems for studying parallel evolution by natural selection. Parallel adaptation occurs in the context of several viral behaviours, including cross-species transmission, drug resistance, and host immune escape, and its existence suggests that at least some aspects of virus evolution and emergence are repeatable and predictable. We introduce examples of virus parallel evolution and summarise key concepts. We outline the difficulties in detecting parallel adaptation using virus genomes, with a particular focus on phylogenetic and structural approaches, and we discuss future approaches that may improve our understanding of the phenomenon.

Parallel evolution in the emergence of highly pathogenic avian influenza A viruses

“…For the H5NX subtype, 2/10 of HAPMs were identified as PSS (see Supplementary Table 1 for details). At first impression, this suggests that most HAPMs significantly associated with the HP phenotype are not a consequence of positive selection 14,17 . However, some HAPMs may be selectively neutral in the absence of a pCS (LP phenotype), but offer a positive effect associated with a pCS (HP phenotype).…”

“…Parallel evolution describes repeated evolutionary changes leading to the same phenotype or genotype in independent populations, and can result from adaptation by natural selection to similar selective pressures or ecological niches 13,14 . We use the term 'parallel molecular evolution' to refer to the convergent or parallel molecular genetic changes that lead to the emergence of same phenotype 15 .…”

The early evolution of oral poliovirus vaccine is shaped by strong positive selection and tight transmission bottlenecks

“…Whereas wild polioviruses and other endemic RNA viruses may already exist near local fitness peaks, OPV is significantly attenuated and is under intense pressure to climb the fitness landscape by accessing available high-impact mutations (9). OPV is also unique in that each population starts from the same founder genetic sequence, making parallel trajectories more likely to occur (38).…”

“…The dN/dS ratio is an imperfect metric for detecting selection, particularly within hosts, and it is unable to identify positive selection of mutations in noncoding regions (36). While changes in frequency of viral variants can be caused by multiple evolutionary forces, observing the same mutation arise in independent viral populations is suggestive of positive selection (37,38). We Figure 3C).…”

Virus population dynamics examined with experimental model systems

“…In contrast, once the constraints inherent to functional cells and viruses are in place, the system might be forced to enter a route conductive to a seemingly deterministic behavior (see Chapter 1 for the time frame in which the increasingly chemical and precellular complexity evolved on Earth). The fact that RNA viruses can accumulate mutations at about one million faster rate than most differentiated organisms (that is, that they represent exceedingly accelerated versions of biological evolution) may underlie unpredictable versus reproducible evolution (Gutierrez et al, 2019), decanted by factors that are not well understood. It is tempting to make a connection between virus-cell coevolution in cell culture and the models of virus origins that contemplated vesicle-wrapped primitive cellular and viral entities (Section 1.5.5 in Chapter 1).…”