On the Causes of Rapid Diversification in the Páramos: Isolation by Ecology and Genomic Divergence in Espeletia

How diversity arises and what is the relative role of allopatric and ecological divergence are among the most persistent questions in evolution and ecology. Here, we assessed whether ecological divergence has enhanced the diversification of the Neotropical alpine plant complex Espeletia, also known as frailejones. This genus has one of the highest diversification rates ever reported and is distributed in the world’s fastest evolving biodiversity hotspot, the Páramo (Neotropical alpine grasslands at elevations of c. 2800–4700 m). Our goal was to determine whether ecology plays a role in divergence within the Espeletia complex by quantifying genome-wide patterns of ecological divergence. We characterized 162 samples of the three most common and contrasting ecotypes (distinct morphotypes occupying particular habitats) co-occurring in six localities in the northern Andes using Genotyping by Sequencing. Contrasting ecotypes were caulescent cloud forest populations, caulescent populations from wind-sheltered and well-irrigated depressions and acaulescent populations from wind-exposed drier slopes. We found high polymorphism with a total of 1,273 single nucleotide polymorphisms (SNPs) that defined the relationships among nine genetic clusters. We quantified allelic associations of these markers with localities and habitats using 18 different general and mixed-effects statistical models that accounted for phylogenetic distance. Despite that these models always yielded more SNPs associated with the localities, markers associated with the habitat types were recovered too. We found strong evidence for isolation-by-distance (IBD) across populations despite rampant gene flow, as expected for plant groups with limited seed dispersal. Contrasts between populations of different habitat types showed that an isolation-by-environment (IBE) trend emerged and masked the IBD signal. Maximum likelihood estimation of the number of migrants per generation (N(e)m) among ecotypes confirmed the IBE pattern. This result illustrates the importance of mountains’ environmental variation at a local scale in generating rapid morphological radiations and maintaining multiple adaptations in a fast-evolving ecosystem like the Páramo.