Introduction
Watermelon (Citrullus lanatus (Thunb.) Matsum. & Nakai) is a horticultural species of high economic importance, accounting for nearly 103,9 million metric tons of global fruit production in 2018 from 3.2 million ha (Faostat, 2017). Over the last two decades, questions regarding the origin and taxonomy ofCitrullus spp. have fuelled numerous studies to clarify phylogenetic relationships and nomenclature, identify wild relatives, and determine both centers of origin and divergence times (Jarret et al., 1997; Jarret & Newman, 2000; Levi et al., 2001; Dane et al., 2004; Levi et al., 2004; Levi & Thomas, 2005; Dane & Liu, 2007; Dane et al., 2007; Solmaz & Sari, 2009; Dje et al., 2010; Solmaz et al., 2010; Nesom, 2011; Levi et al., 2013; Mujaju et al., 2013; Hammer & Gladis, 2014; Chomicki & Renner, 2015; Renner et al., 2019; Chomicki et al., 2020). Despite these efforts, uncertainty vis-à-vis these questions remains as no wild relatives were found neither in west nor in northern east Africa; and comparatively few studies have focused on the distribution of the genetic variation within Citrullus or the likely colonization routes of various species within the genus.
The challenge of tracing the historical colonization routes of watermelon was for many years confounded by significant taxonomic confusion among species, subspecies, and varieties, all of which exhibit high morphological diversity. Citrullus Schrad. ex Eckl & Zeyh. is one of 95 genera of Cucurbitaceae (Jeffrey, 2005; Kocyan et al., 2007; Schaefer & Renner, 2011b; Schaefer & Renner, 2011a). To date there seems to be a consensus regarding its complex taxonomy. According to recent research, including phylogenetic analyses and nomenclatural reviews (Renner et al., 2014; Chomicki et al., 2020) as well as a phenetic comparison within the genus (Achigan-Dako et al., 2015),Citrullus encompasses the following seven species: 1) the widely cultivated C. lanatus , a juicy fruit found in tropical and subtropical climates including var. cordophanus (Ter-Avan.) Fursa; 2) the tsamma melon C. amarus Schrad syn. C. cafferSchrad. or C. lanatus var. citroides (Bailey) Mansf., which grows in southern Africa (Whitaker & Bemis, 1976); 3) the egusi melon C. mucosospermus Fursa, previously referred to as a subtaxon of C. lanatus by many authors but which was raised to specific rank many decades ago (Fursa, 1972; Fursa, 1981; Fursa, 1983); 4) the bitter appleC. colocynthis (L.) Schrad., a perennial species growing in sandy areas throughout northern Africa and Near-East ; 5) C. ecirrhosusCogn., another perennial wild species (De-Winter, 1990); 6) C. rehmii , a wild annual species, with small fruits used for feeding desert animals; and 7) C. naudinianus (Sond.) Hook.f. from the Namib-Kalahari region, previously placed in the genus Acanthosicyos Welw. ex Hook. f. and sister group to all other species. Citrullus eccirhosus , C . rehmii, and C. naudinianus,currently, are considered endemic and restricted to the desert region of Namibia with very little intraspecific variation (Dane & Lang, 2004); this understanding may change with more extensive sampling.
Given recent clarification of Citrullus taxonomy, it is appropriate to revisit the question of genealogy. In a recent phylogenetic study, Chomicki and Renner (2015) indicated west Africa as the possible center of origin ofC. lanatus , a claim at odds with earlier assertions. Indeed, whereas some experts believe watermelon originated from southern Africa, based on the distribution of wild relatives in the Namibian desert (Bates & Robinson, 1995), others point to northern or north-east Africa, especially the Nile river area in Sudan, as the likely center of origin based on archaeological data (Wasylikowa & Van Der Veen, 2004; Paris, 2015; Renner et al., 2019). According to these latter studies, very few archaeological records of watermelon are known from southern Africa; and all date to a relatively recent period between the 8th and 13th centuries A.D. Furthermore, a cultigen is known to have been cultivated in the Nile Valley when farming was not yet practiced in southwest Africa (Zohary & Hopf, 2000). In contrast, archaeological records from West Africa are scanty, except for the presence of one endemic cultivated species (C. mucosospermus ) previously deemed to be a subspecies or variety of C. lanatus(Nesom, 2011; Hammer & Gladis, 2014; Renner et al., 2014; Achigan-Dako et al., 2015).
The fundamental questions remain: how did watermelon spread throughout the world if it has originated from west or north-east Africa? How did the extant cultigens distribute throughout the world and how do they relate to wild types such as C. colocynthis or C. amarus ? To contribute to our understanding of these questions, this paper presents a chloroplast phylogeography of Citrullus lanatus and three related species, one cultivated (C. mucosospermus ) and two wild (C. amarus and C. colocynthis ), using a large sample size collected from four continents. The objective is to characterize the geographical distribution of Citrullus haplotypes and shed specific light of the chloroplast sequence evolution of C. lanatus , hypothesizing that such information will help clarify our understanding of the history of this globally significant agricultural species.