Phylogenomic Analysis of the Explosive Adaptive Radiation of the Espeletia Complex (Asteraceae) in the Tropical Andes

International audienceThe subtribe Espeletiinae (Asteraceae), endemic to the high-elevations in the Northern Andes, exhibits anexceptional diversity of species, growth-forms, and reproductive strategies. This complex of 140 species includes large trees,dichotomous trees, shrubs and the extraordinary giant caulescent rosettes, considered as a classic example of adaptation intropical high-elevation ecosystems. The subtribe has also long been recognized as a prominent case of adaptive radiation,but the understanding of its evolution has been hampered by a lack of phylogenetic resolution. Herein, we produce the firstfully resolved phylogeny of all morphological groups of Espeletiinae, using whole plastomes and about a million nuclearnucleotides obtained with an originalde novoassembly procedure without reference genome, and analyzed with traditionaland coalescent-based approaches that consider the possible impact of incomplete lineage sorting and hybridization onphylogenetic inference. We show that the diversification of Espeletiinae started from a rosette ancestor about 2.3 Ma, afterthe final uplift of the Northern Andes. This was followed by two independent radiations in the Colombian and VenezuelanAndes, with a few trans-cordilleran dispersal events among low-elevation tree lineages but none among high-elevationrosettes. We demonstrate complex scenarios of morphological change in Espeletiinae, usually implying the convergentevolution of growth-forms with frequent loss/gains of various traits. For instance, caulescent rosettes evolved independentlyin both countries, likely as convergent adaptations to life in tropical high-elevation habitats. Tree growth-forms evolvedindependently three times from the repeated colonization of lower elevations by high-elevation rosette ancestors. The rateof morphological diversification increased during the early phase of the radiation, after which it decreased steadily towardsthe present. On the other hand, the rate of species diversification in the best-sampled Venezuelan radiation was on averagevery high (3.1 spp/My), with significant rate variation among growth-forms (much higher in polycarpic caulescent rosettes).Our results point out a scenario where both adaptive morphological evolution and geographical isolation due to Pleistoceneclimatic oscillations triggered an exceptionally rapid radiation for a continental plant group. [Adaptive radiation; caulescentrosette; explosive diversification; Espeletiinae; hybridization; paramo; phylogenomics; tropical high-elevation.