A phylogenomic dive into giant genomes: unravelling the evolutionary history of Tmesipteris (Psilotales).

Abstract

Genomic gigantism is rare and reaches its extreme in fork ferns (genus Tmesipteris, Psilotaceae, Psilotales), whose unresolved systematics have obscured the roles of polyploidy, hybridization, and repetitive element dynamics in forming exceptionally large genomes. Here, we address this issue by developing a custom target-capture probe set (288 nuclear orthologs), integrating time-calibrated multispecies coalescent analysis and biogeographic modelling with nuclear DNA content estimates, cytotype inference and repeatome profiles to better understand the evolution of the group. We recovered a well-resolved backbone, consistent with a Paleocene split of Psilotaceae into two genera, and an Oligocene crown diversification of Tmesipteris into two strongly supported lineages (Pacific and Tasman clades). Diversification seems to coincide with the emergence of island habitats across Zealandia and New Caledonia, consistent with long-distance dispersal, founder events, and life-form shifts. Nuclear and plastid discordance is for the most part concentrated within the Pacific clade, indicative of potential recurrent hybridization and/or incomplete lineage sorting (ILS). Genome analyses reveal multiple independent whole-genome multiplications, producing several octoploid lineages and intraspecific cytotype diversity. Repetitive DNA content is exceptionally high, with clade-specific dynamics of transposable elements and satellite DNA. We confirm the taxonomic independence of T. oblanceolata from T. truncata, and identify two putative nothotaxa in the Pacific clade, plus a distinct Fijian taxon closely allied to T. alticola, which could represent an undescribed species. Altogether, these findings point to whole-genome multiplication, hybridization, inter-island dispersal, and repetitive DNA accumulation as primary drivers of diversification and genome gigantism in Tmesipteris.