Revealing Speciation Mechanisms Across Endemic Southern Andean Lilies (Phycella, Hippeastreae, Amaryllidaceae) in the Chilean Biodiversity Hotspot

Abstract

Cryptic speciation, an endemic problem in biodiversity hotspots, arises as a result of an uncoupling among three processes: lineage splitting, morphological diversification, and ecological divergence during rapid speciation. We studied speciation processes in Phycella (Amaryllidaceae), a clade mostly restricted to the Chilean Biodiversity Hotspot, aiming to differentiate the relative roles of geographic and ecological speciation as well as the role of secondary gene flow in this radiation. We sampled a total of 137 individuals from 47 populations, including all described taxa throughout the geographic range of the group. Using 884 nuclear genes (1125 exons) and near-complete plastomes through hybrid capture, we resolved the phylogeny of Phycella with high support and demonstrated substantial phylogenetic resolution at the population level. Analyses of niche overlap among species and nuclear clades suggest that the diversification of Phycella was associated with niche divergence, supporting a predominantly geographic mode of speciation in the group, likely driven by the mountainous landscape characteristic of the central area of the Chilean Biodiversity Hotspot. Phylogenetic network and modelling approaches identified major cytonuclear discord, attributable to proximity-based secondary gene flow among species, largely restricted to cytoplasmic DNA. Finally, we present a major integrative taxonomic proposal that divides Phycella into 18 species on the basis of molecular, morphological, and ecological data. Overall, our results highlight the relevance of the mountainous landscape of central Chile to promote diversification in Phycella, and ours is among a few studies on speciation for an endemic element of the Chilean Biodiversity Hotspot.