A domesticated totivirus-like tandem array undergoes interspecific transfer and asymmetric evolution.

Authors

Derek J Taylor, Dominic A Tringali

Published in

Molecular biology and evolution. Oct 31, 2026. Epub Oct 31, 2026.

Abstract

Functional genes derived from nonretroviral RNA viruses are generally expected to evolve more slowly following integration into host genomes. Here, we characterize STORM (Scheffersomyces Totivirus-like ORF Repeat Module), a tandem array of four totivirus-derived ORFs (TLC1-TLC4) maintained in wood- and insect-associated yeasts for at least 15 million years. STORM has nevertheless accumulated greater amino-acid divergence than sampled exogenous totiviruses. Host calibrated rate analyses estimated that STORM evolved approximately seven-fold faster than related exogenous viral lineages. Evolution within the array was asymmetric. RELAX identified strong gene-wide relaxation in TLC4 (K = 0.29), whereas BUSTED detected no episodic positive selection. Despite this relaxation, TLC4 retained predicted decapping-associated residues, with evidence of purifying selection at several positions. Structural predictions indicated that STORM proteins retain a totivirus-like architecture, and RNA-seq comparisons revealed paralog-specific expression. Among 3,527 complete nuclear gene trees, none recovered all relationships defining any of the three STORM discordances with strong support, indicating that these patterns are exceptional relative to the nuclear genomic background. Local synteny and preservation of the four-copy array further support three interspecific transfers. In the best-supported transfer, STORM was flanked by an ATP10 pseudogene and a transposase pseudogene from YEET, a newly identified Tc1/mariner-like transposon family. Both pseudogenes grouped phylogenetically with the inferred donor clade, and YEET1a-like terminal inverted repeats at the locus were characteristic of that clade. STORM therefore illustrates the selective maintenance, rapid asymmetric evolution, and horizontal mobility of a nonretroviral paleoviral array.

PMID:
42963186
Bibliographic data and abstract were imported from PubMed on 31 Oct 2026.

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