The impact of early Quaternary climate change on the diversification and population dynamics of a South American cactus species

Aim: Climatic oscillations have been suggested to promote speciation and changes in species distributions, mostly in connection with the Last Glacial Maximum (LGM). However, the LGM is just the most recent of the 20+ glacial-interglacial periods that characterise the Quaternary. Here, we investigate the role of climatic changes and geomorphological features in shaping the evolution, distribution and population dynamics of the South American cactus Cereus hildmannianus. Location: South-eastern South America. Methods: We built a large fossil-calibrated phylogeny for cacti (family Cactaceae), comprising 128 species distributed in all subfamilies, using a Bayesian relaxed clock. We used the results to derive a secondary calibration for a population-level phylogeny in C. hildmannianus. We amplified two plastid (trnQ-5'rps16 and psbJ-petA) and one nuclear marker (PhyC) for 24 populations. We estimated population dynamics, ancestral areas, and species distribution models to infer the clade's evolutionary history in time and space. Results: Our results show a major population divergence of C. hildmannianus at c. 2.60 Ma, which is strikingly coincident with the transition of the Pliocene-Pleistocene and onset of Quaternary glaciations. This was followed by a complex phylogeographic scenario involving population expansions across ecologically diverse regions. Main conclusions: Contrary to the dominant research focus on the LGM, our study indicates a major impact of the first Quaternary glaciation on the distribution and population divergence of a South American plant species. Further intraspecific events seem related to successive climatic changes and geomorphology, including the development of the coastal plain and its peculiar diversity. We propose that the first Quaternary glaciation acted as a major evolutionary bottleneck, whereby many warm-adapted lineages succumbed, while those that survived could diversify and better cope with subsequent climatic oscillations.