The different routes of parallel evolution in epiarenic growth in a hyperarid desert environment

The Atacama Desert, one of the driest and oldest regions on Earth, represents an extreme environment that has driven remarkable adaptive evolution over millions of years. Within this setting, the genus Tillandsia comprises specialists capable of surviving at the dry limit of plant life. These species exhibit crassulacean acid metabolism (CAM), lack functional roots, and possess trichomes adapted for water and nutrient absorption. Of the more c. 750 known Tillandsia species, nine occur in the Chilean-Peruvian Atacama Desert, where they colonize bare sand surfaces (epiarenic growth) under hyperarid conditions without significant rainfall, relying solely on nocturnal fog for moisture. Despite their striking adaptations, the evolutionary mechanisms and timing underlying the emergence of epiarenic growth remain poorly understood. Here, we reconstructed a maximum-likelihood phylogeny based on 278 plastome sequences of Tillandsioideae and other Bromeliaceae subfamilies to study respective sister species relationships. Further, divergence time estimates for the origin of epiarenic Tillandsia were estimated using Bayesian inference in BEAST2. In addition, we analyzed variation in orthologous copies of the nuclear-encoded Agt1 gene to test for interspecific and interploidal gene flow among epiarenic taxa and their closest relatives. This gene has been previously established as a barcoding marker in bromeliads. The results indicate that epiarenic Tillandsia evolved multiple times independently from the Late Pliocene through the Pleistocene, consistent with a long-term hyperarid evolutionary arena promoting extreme adaptations. Moreover, evidence for frequent interspecific hybridization and gene flow suggests that hybridization may have also contributed to the long-term success of epiarenic Tillandsia species and is reflecting also the spatio-temporal dynamics of the Atacama's hyperarid landscapes during the Pleistocene.