Resolving the stasis-dynamism paradox: Genome evolution in tree ferns.

Abstract

The paradox of evolutionary stasis and dynamism-how morphologically static lineages persist through deep geological periods despite environmental fluctuations-remains unresolved in evolutionary biology. Here, we present chromosome-scale genomes for three ecologically divergent species (including both arborescent and non-arborescent growth forms) within Cyatheaceae, an ancient tree fern family characterized by morphological conservation dating back to the Jurassic era. Our results revealed substantial yet cryptically regulated genomic dynamism. A shared Jurassic whole-genome duplication (∼154 Ma) conferred dual adaptive advantages: initially buffering tree ferns against Late Jurassic climatic extremes through retention of stress-response genes, and subsequently facilitating niche diversification and phenotypic innovation via lineage-specific repurposing of duplicate genes. Arborescent lineages preferentially retained duplicates involved in cell wall biogenesis, essential for structural reinforcement and lignification, while non-arborescent forms conserved paralogs linked to metabolic resilience and defense. Alongside slow substitution rates, we detected cryptic genome dynamism mediated primarily by bursts of transposable elements, leading to genome size variations, chromosomal rearrangements, and localized innovation hotspots with elevated evolutionary rates. The concerted expansion and expression of lignification-related genes, coordinated with light signaling components, suggest a potential evolutionary mechanism integrating light perception with shade-adaptation and lignification, facilitating arborescent adaptation in angiosperm-dominated understories. Our findings redefine evolutionary stasis as a dynamic equilibrium, sustained by regulatory plasticity and localized genomic innovation within a conserved morphological framework. This study offers a novel genomic perspective on the long-term persistence and evolution of ancient plant lineages, demonstrating how regulated genomic dynamism enables adaptive diversification while sustaining morphological conservatism.