Specialized herbivory in fossil leaves reveals convergent origins of nyctinasty

Plants can move in various complex ways in response to external stimuli. These mechanisms include responses to environmental triggers, such as tropic responses to light or gravity and nastic responses to humidity or contact. Nyctinasty, the movements involving circadian rhythmic folding at night and opening at daytime of plant leaves or leaflets, has attracted the attention of scientists and the public for centuries. In his canonical work entitled The Power of Movement in Plants, Charles Darwin carried out pioneering observations to document the diverse range of movements in plants. His systematic examination of plants showing ‘‘sleep [folding] movements of leaves’’ led him to conclude that the legume family (Fabaceae) includes many more nyctinastic species than all other families combined. Darwin also found that a specialized motor organ, the pulvinus, is responsible for most sleep movements of plant leaves, although differential cell division and the hydrolysis of glycosides and phyllanthurinolactone also facilitate nyctinasty in someplants. However, the origin, evolutionary history, and functional benefits of foliar sleep movements remain ambiguous owing to the lack of fossil evidence for this process. Here, we document the first fossil evidence offoliar nyctinasty based on a symmetrical style of insect feeding damage (Folifenestra symmetrica isp. nov.) in gigantopterid seed-plant leaves from the upper Permian (c. 259–252 Ma) of China. The pattern of insect damage indicates that the host leaves were attacked when mature but folded. Our finding reveals that foliar nyctinasty extends back to the late Paleozoic and evolved independently among various plant lineages.This study was supported jointly by the Strategic Priority Research Program of Chinese Academy of Sciences (XDB26000000), the Second Tibetan Plateau Scientific Expedition and Research (2019QZKK0706), and the Key Research Program of the Institute of Geology and Geophysics, Chinese Academy of Sciences (IGGCAS-201905). S.M. was funded by grants from the Swedish Research Council (VR grant numbers 2018-04527 and 2022-03920).