On the origins and domestication of the olive: a review and perspectives

Annals of Botany 121: 385–403, 2018 doi:10.1093/aob/mcx145, available online at www.academic.oup.com/aob REVIEW On the origins and domestication of the olive: a review and perspectives Guillaume Besnard1,*, Jean-Frédéric Terral2,3 and Amandine Cornille4,5 CNRS-UPS-ENSFEA-IRD, EDB, UMR 5174, Université Paul Sabatier, Bât. 4R1, 31062 Toulouse Cedex 9, France, 2ISEM, UMR 5554, CNRS-Université de Montpellier-IRD-EPHE, Equipe Dynamique de la Biodiversité, Anthropo-écologie, Place Eugène Bataillon, CC065, 34095 Montpellier Cedex 5, France, 3International Associated Laboratory (LIA, CNRS) EVOLea, 4 Center for Adaptation to a Changing Environment, ETH Zürich, 8092 Zürich, Switzerland and 5GQE - Le Moulon, INRA, Univ. Paris-Sud, CNRS, AgroParisTech, Université Paris-Saclay, 91190 Gif-sur-Yvette, France *For correspondence. E-mail 1 Returned for revision: 7 July 2017 Editorial decision: 21 August 2017 Accepted: 12 october 2017 Published electronically: 30 January 2017 • Background 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. • Scope 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. • Conclusion 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. Key words: Adaptation, phylogeography, introgression, Oleaceae, pathogen, microbes INTRODUCTION The cultivated olive (Olea europaea L. subsp. europaea var. europaea; Box 1) is considered to be the most iconic tree of the Mediterranean Basin, with origins linked to the emergence of some of the most ancient civilizations, about six millennia ago (Loumou and Giourga, 2003; Kaniewski et al., 2012; Zohary et al., 2012). In classical times, olive cultivation expanded to new regions and intensified around the Mediterranean Basin and beyond (InfanteAmate et al., 2016). Today, hundreds of olive varieties are grown to produce high-quality fruit for oil and for table consumption (Bartolini et al., 2005), but debate about their origins continues (e.g. Díez et al., 2015; Besnard and Rubio de Casas, 2016). The relationships between cultivated olives and wild Mediterranean olives [Olea europaea subsp. europaea var. sylvestris (Mill.) Leh., or the so-called oleaster; Box 1] are also unclear. The multiple uses of cultivated and wild olive trees, as sources of food, wood and cattle fodder, explain the expansion of olive groves with the spread of human civilization. The dual role of olives as both wild elements of the Mediterranean vegetation and as a cultivated crop has posed challenges to researchers trying to decipher the domestication history of this species. It also remains difficult to distinguish between feral (escaped from cultivation) and genuinely wild Mediterranean olives, even with the recently developed use of genetic and phenotypic traits to assist identification (Box 1). Such a tenuous domestication syndrome is a key issue that has affected research carried out on domestication of the olive, but also of other Mediterranean woody crops such as grape and date palm (Zohary et al., 2012). For all these reasons, there has long been speculation about the origin and domestication history of olives, mostly based on botanical data (e.g. Newberry, 1937; Chevalier, 1948; Turrill, 1951). The recent accumulation of paleobotanical, archeological, historical and molecular data (e.g. Terral et al., 2004a; Carrión et al., 2010; Kaniewski et al., 2012; Besnard et al., 2013b; Margaritis, 2013; Newton et al., 2014; Dίez et al., 2015; Rugini et al., 2016; see Supplementary Data Table S1 for current available genetic data) has made a crucial re-evaluation of the biogeography of wild olives and the history of their © The Author(s) 2017. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: . Received: 4 May 2017 Besnard et al. — On the origins and domestication of the olive 386 Box 1. Ecology of wild olives and the domesticated status of cultivated olives Six wild olive subspecies are currently recognized (Fig. B1 A) and considered to be primary genetic resources for cultivated olive breeding (Zohary, 1994; Green, 2002). They are diploid, except for subspp. maroccana and cerasiformis, which are polyploid (6x and 4x, respectively; Besnard et al., 2008). In tropical and sub-tropical regions, non-Mediterranean olives (subspp. cuspidata and laperrinei) harbour small fruits (diameter generally <8 mm; Médail et al., 2001) and trees usually grow in mountainous areas (Fig. B1 B). The African olive (subsp. cuspidata) can also invade anthropogenic habitats, as observed in Australia (Fig. B1 C). The taxonomy of the olive complex is relatively well supported by genetic data (e.g. Rubio de Casas et al., 2006; Besnard et al., 2007). Each subspecies harbours specific plastid lineages/sub-lineages, with several lineages/sub-lineages detected within the four diploid subspecies. The 13 plastid lineages/sub-lineages are specified on the map (Fig. B1 A). B A E1-e M-c E2 & E3 M-m M-g1 M-g2 E1-/1 C1 E1-/3 C2 C1 E1-/2 C2 A C subsp. cerasiformis subsp. cuspidata subsp. europaea subsp. guanchica subsp. laperrinei subsp. marocanna A (...truncated)