C ₄ photosynthesis is a series of anatomical and biochemical modifications to the typical C ₃ pathway that increases the productivity of plants in warm, sunny, and dry conditions. Despite its complexity, it evolved more than 62 times independently in flowering plants. However, C ₄ origins are absent from most plant lineages and clustered in others, suggesting that some characteristics increase C ₄ evolvability in certain phylogenetic groups. The C ₄ trait has evolved 22–24 times in grasses, and all origins occurred within the PACMAD clade, whereas the similarly sized BEP clade contains only C ₃ taxa. Here, multiple foliar anatomy traits of 157 species from both BEP and PACMAD clades are quantified and analyzed in a phylogenetic framework. Statistical modeling indicates that C ₄ evolvability strongly increases when the proportion of vascular bundle sheath (BS) tissue is higher than 15%, which results from a combination of short distance between BS and large BS cells. A reduction in the distance between BS occurred before the split of the BEP and PACMAD clades, but a decrease in BS cell size later occurred in BEP taxa. Therefore, when environmental changes promoted C ₄ evolution, suitable anatomy was present only in members of the PACMAD clade, explaining the clustering of C ₄ origins in this lineage. These results show that key alterations of foliar anatomy occurring in a C ₃ context and preceding the emergence of the C ₄ syndrome by millions of years facilitated the repeated evolution of one of the most successful physiological innovations in angiosperm history.

The location and timing of domestication of the olive tree, a key crop in Early Mediterranean societies, remain hotly debated. Here, we unravel the history of wild olives (oleasters), and then infer the primary origins of the domesticated olive. Phylogeography and Bayesian molecular dating analyses based on plastid genome profiling of 1263 oleasters and 534 cultivated genotypes reveal three main lineages of pre-Quaternary origin. Regional hotspots of plastid diversity, species distribution modelling and macrofossils support the existence of three long-term refugia; namely the Near East (including Cyprus), the Aegean area and the Strait of Gibraltar. These ancestral wild gene pools have provided the essential foundations for cultivated olive breeding. Comparison of the geographical pattern of plastid diversity between wild and cultivated olives indicates the cradle of first domestication in the northern Levant followed by dispersals across the Mediterranean basin in parallel with the expansion of civilizations and human exchanges in this part of the world.

Unravelling domestication processes is crucial for understanding how species respond to anthropogenic pressures, forecasting crop responses to future global changes and improving breeding programmes. Domestication processes for clonally propagated perennials differ markedly from those for seed-propagated annual crops, mostly due to long generation times, clonal propagation and recurrent admixture with local forms, leading to a limited number of generations of selection from wild ancestors. However, additional case studies are required to document this process more fully. The olive is an iconic species in Mediterranean cultural history. Its multiple uses and omnipresence in traditional agrosystems have made this species an economic pillar and cornerstone of Mediterranean agriculture. However, major questions about the domestication history of the olive remain unanswered. New paleobotanical, archeological, historical and molecular data have recently accumulated for olive, making it timely to carry out a critical re-evaluation of the biogeography of wild olives and the history of their cultivation. We review here the chronological history of wild olives and discuss the questions that remain unanswered, or even unasked, about their domestication history in the Mediterranean Basin. We argue that more detailed ecological genomics studies of wild and cultivated olives are crucial to improve our understanding of olive domestication. Multidisciplinary research integrating genomics, metagenomics and community ecology will make it possible to decipher the evolutionary ecology of one of the most iconic domesticated fruit trees worldwide. The olive is a relevant model for improving our knowledge of domestication processes in clonally propagated perennial crops, particularly those of the Mediterranean Basin. Future studies on the ecological and genomic shifts linked to domestication in olive and its associated community will provide insight into the phenotypic and molecular bases of crop adaptation to human uses.