Evolutionary Virology at 40

Abstract

RNA viruses are diverse, abundant, and rapidly evolving. Genetic data have been generated from virus populations since the late 1970s and used to understand their evolution, emergence, and spread, culminating in the generation and analysis of many thousands of viral genome sequences. Despite this wealth of data, evolutionary genetics has played a surprisingly small role in our understanding of virus evolution. Instead, studies of RNA virus evolution have been dominated by two very different perspectives, the experimental and the comparative, that have largely been conducted independently and sometimes antagonistically. Here, we review the insights that these two approaches have provided over the last 40 years. We show that experimental approaches using in vitro and in vivo laboratory models are largely focused on short-term intrahost evolutionary mechanisms, and may not always be relevant to natural systems. In contrast, the comparative approach relies on the phylogenetic analysis of natural virus populations, usually considering data collected over multiple cycles of virus-host transmission, but is divorced from the causative evolutionary processes. To truly understand RNA virus evolution it is necessary to meld experimental and comparative approaches within a single evolutionary genetic framework, and to link viral evolution at the intrahost scale with that which occurs over both epidemiological and geological timescales. We suggest that the impetus for this new synthesis may come from methodological advances in next-generation sequencing and metagenomics.

Analysis of Rapidly Emerging Variants in Structured Regions of the SARS-CoV-2 Genome

“…DNA sequencing technology has progressed remarkably since the SARS outbreak of 2003 (Geoghegan and Holmes 2018;Zhang et al 2018). It is now routine to determine the sequence of the ~30 kilobase viral genome using high throughput sequencing technology (Wu et al 2020).…”

Long-term virus evolution in nature

“…Phylogenetic reconstructions based on nucleotide (and deduced amino acid) sequence alignments are generally possible with selected genes of relatively close viruses (i.e., that belong to the same family). The main methods used to derive evolutionary trees are: maximum parsimony, distance, ML, Bayesian methods of phylogenetic inference, and splits-tree analysis [reviewed in (Eigen, 1992;Page and Holmes, 1998;Mount, 2004;Salemi and Vandamme, 2004;Sullivan, 2005;Holmes, 2008;Beale et al, 2018;Geoghegan and Holmes, 2018)] (Table 7.3).…”

The phylogenetic approach for viral infectious disease evolution and epidemiology: An updating review

“…We consider first RNA viruses, like influenza and HIV, which pose grave risk to public health worldwide. These fast evolving viruses continuously adapt to the highly variable environments they live, by evading host immune responses and altering the severity of disease . Influenza viruses, that infects about one‐fifth of the worldwide human population each year, are characterized by a very rapid evolution, resulting from mutations or genetic reassortment with other of influenza viruses, such as pig, horses, and birds .…”