Introns as Protective Buffers Against Transposable Elements Invasion During Genome Gigantism in a Newt

Abstract

Genome gigantism has long been linked to recurrent bursts of transposable element (TE) activity, yet how such bursts reshape gene architecture over evolutionary time remains poorly understood. By comparing two independently assembled genomes of the Iberian ribbed newt Pleurodeles waltl (20.3 Gb)—generated in Europe and Japan—with the compact genome of Xenopus tropicalis (1.5 Gb), we uncover evidence for both past and ongoing TE bursts during newt genome expansion. Analyses of multicopy genes reveal a spectrum of evolutionary outcomes driven by successive waves of intronic TE invasion. While some genes remain functional despite massive gene body inflation through efficient splicing-mediated removal of TE insertions, others undergo transcriptional silencing, followed by mutation accumulation, pseudogenization, and progressive disorganization of exon–intron architecture. Direct comparison between the two P Pleurodeles waltl assemblies demonstrates that TE insertions continue to occur, indicating that genome expansion is an active, ongoing process. We further identify Bou1, a testis-specific, TE-derived locus whose expression coincides with germline-associated TE activity. Together, these results depict genome gigantism as a punctuated yet persistent process and suggest that introns act as protective buffers against TE invasion, delaying gene decay until selective constraints are relaxed.