Evolutionary rates vary widely among sites in protein sequences, reflecting differences in functional constraints across residues. Individual sites can also experience lineage-specific shifts in substitution rates--a process known as heterotachy--when selective pressures change during evolution. Although such temporal variation has long been recognized, the mechanisms underlying lineage-specific rate shifts and the factors shaping their distribution across protein families remain poorly understood. Here we map site-specific rate shifts across thousands of orthologous protein families spanning the tree of life. Among more than 1.8 million aligned amino-acid sites, over one quarter show evidence of lineage-specific rate changes. Rate shifts are more frequent in families with deep evolutionary origins, including those tracing back to LUCA, whereas younger clade-specific families generally show lower proportions of rate-shifting sites. We next examined whether local structural features predict where rate shifts occur. Residue burial shows only a weak association with rate-shift probability, and its direction differs across domains, with buried residues enriched for rate shifts in Archaea but surface-exposed residues showing slightly higher probabilities in Eukaryota. Moreover, rate-shifting sites rarely form spatial clusters within protein structures, indicating that structural constraints do not globally determine their locations. Despite their widespread occurrence, rate-shifting sites have limited impact on phylogenetic reconstruction beyond random site variation. Together, these results show that lineage-specific rate shifts are a pervasive feature of protein evolution shaped primarily by evolutionary ancestry and phylogenetic depth.
Durak, M. R., Renaud, E., Dutheil, J. Y.
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