Phylogenomics and Biogeography of the Mammilloid Clade Revealed an Intricate Evolutionary History Arose in the Mexican Plateau

SIMPLE SUMMARY: Cacti account for nearly 1440 species, most of them native to the American continent. These succulent plants are the most ubiquitous elements of the arid ecosystems. Mexico harbors the highest number of cacti species in the world (45%). Unfortunately, many of them are threatened by human activities. Although having this biodiversity relevance, presently the evolutionary processes of cacti have been poorly studied. Because the biological and conservation unit is the species, evolutionary studies provide relevant information. In this study, we analyzed how and when past events shaped the evolutionary relationships of 103 species. Our results showed that from 4.5 million years ago the arid regions of Mexico were the locations for abundant cacti speciation. From these lands, cacti have colonized most of the Mexican territories, the southern regions of the United States, as well as the Caribbean. The evolution of these plants was probably promoted by past temperatures that were comparable to the present ones. We identified different speciation and dispersal events in these fascinating plants. This study identified the Mexican Plateau as the place where the early stages of the evolutionary history of cacti occurred. ABSTRACT: Mexico harbors ~45% of world’s cacti species richness. Their biogeography and phylogenomics were integrated to elucidate the evolutionary history of the genera Coryphantha, Escobaria, Mammillaria, Mammilloydia, Neolloydia, Ortegocactus, and Pelecyphora (Mammilloid Clade). We analyzed 52 orthologous loci from 142 complete genomes of chloroplast (103 taxa) to generate a cladogram and a chronogram; in the latter, the ancestral distribution was reconstructed with the Dispersal-Extinction-Cladogenesis model. The ancestor of these genera arose ~7 Mya on the Mexican Plateau, from which nine evolutionary lineages evolved. This region was the site of 52% of all the biogeographical processes. The lineages 2, 3 and 6 were responsible for the colonization of the arid southern territories. In the last 4 Mya, the Baja California Peninsula has been a region of prolific evolution, particularly for lineages 8 and 9. Dispersal was the most frequent process and vicariance had relevance in the isolation of cacti distributed in the south of Mexico. The 70 taxa sampled as Mammillaria were distributed in six distinct lineages; one of these presumably corresponded to this genus, which likely had its center of origin in the southern part of the Mexican Plateau. We recommend detailed studies to further determine the taxonomic circumscription of the seven genera.