Darwin's Overlooked Radiation: genomic evidence points to the early stages of a radiation in the Galapagos prickly pear cactus (Opuntia, Cactaceae)

Abstract

The Galapagos Islands are a prime example of a natural laboratory for the study of evolutionary radiations. While much attention has been devoted to iconic species like Darwins finches 1-4, the islands offer an equally unique but often overlooked opportunity for plant radiations 5. Yet, compared to their animal counterparts, our understanding of the patterns and processes underpinning Galapagos plant radiations remains relatively limited 6,7. We present evidence of the early stages of a radiation in prickly-pear cactus (Opuntia, Cactaceae), a plant lineage widespread across the archipelago. Phylogenomic and population genomic analyses show that notwithstanding overall low genetic differentiation across populations, there is marked geographic structure that is broadly consistent with current taxonomy and the dynamic paleogeography of the Galapagos. Because such low genetic differentiation stands in stark contrast to the exceptional eco-phenotypic diversity displayed by cacti across islands, it is plausible that phenotypic plasticity precedes genetic divergence and is the source of adaptive evolution, or that introgression between populations facilitates local adaptation. Models of population relationships including admixture indicate that gene flow is common between certain islands, likely facilitated by dispersal via animals known to feed on Opuntia flowers, fruits, and seeds across the archipelago. Scans of genetic differentiation between populations reveal candidate loci associated with seed traits and environmental stressors, suggesting that a combination of biotic interactions and abiotic pressures due to the harsh conditions characterizing island life in a volcanic, equatorial archipelago may underlie the diversification of prickly-pear cacti. Considered in concert, these results are relevant to both the mechanisms of plant eco-phenotypic differentiation and the evolutionary history and conservation of the Galapagos biota.