Detecting punctuated evolution in SARS-CoV-2 over the first year of the pandemic

The Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) evolved slowly over the first year of the Coronavirus Disease 19 (COVID-19) pandemic with differential mutation rates across lineages. Here, we explore how this variation arose. Whether evolutionary change accumulated gradually within lineages or during viral lineage branching is unclear. Using phylogenetic regression models, we show that ~13% of SARS-CoV-2 genomic divergence up to May 2020 is attributable to lineage branching events (punctuated evolution). The net number of branching events along lineages predicts ~5% of the deviation from the strict molecular clock. We did not detect punctuated evolution in SARS-CoV-1, possibly due to the small sample size, and in sarbecovirus broadly, likely due to a different evolutionary process altogether. Punctuation in SARS-CoV-2 is probably neutral because most mutations were not positively selected and because the strength of the punctuational effect remained constant over time, at least until May 2020, and across continents. However, the small punctuational contribution to SARS-CoV-2 diversity is consistent with the founder effect arising from narrow transmission bottlenecks. Therefore, punctuation in SARS-CoV-2 may represent the macroevolutionary consequence (rate variation) of a microevolutionary process (transmission bottleneck).