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

  • publication
  • 01-11-2018

Pouchon C, Fernández A, Nassar JM, Boyer F, Aubert S, Lavergne S, Mavárez J. Syst Biol. 2018 Nov 1;67(6):1041-1060. doi: 10.1093/sysbio/syy022

The subtribe Espeletiinae (Asteraceae), endemic to the high-elevations in the Northern Andes, exhibits an exceptional 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 in tropical 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 first fully resolved phylogeny of all morphological groups of Espeletiinae, using whole plastomes and about a million nuclear nucleotides obtained with an original de novo assembly procedure without reference genome, and analyzed with traditional and coalescent-based approaches that consider the possible impact of incomplete lineage sorting and hybridization on phylogenetic inference. We show that the diversification of Espeletiinae started from a rosette ancestor about 2.3 Ma, after the final uplift of the Northern Andes. This was followed by two independent radiations in the Colombian and Venezuelan Andes, with a few trans-cordilleran dispersal events among low-elevation tree lineages but none among high-elevation rosettes. We demonstrate complex scenarios of morphological change in Espeletiinae, usually implying the convergent evolution of growth-forms with frequent loss/gains of various traits. For instance, caulescent rosettes evolved independently in both countries, likely as convergent adaptations to life in tropical high-elevation habitats. Tree growth-forms evolved independently three times from the repeated colonization of lower elevations by high-elevation rosette ancestors. The rate of morphological diversification increased during the early phase of the radiation, after which it decreased steadily towards the present. On the other hand, the rate of species diversification in the best-sampled Venezuelan radiation was on average very 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 Pleistocene climatic oscillations triggered an exceptionally rapid radiation for a continental plant group.

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