Some of the World's most valuable crops, including watermelon, honey melon, cucumber, squash, zucchini and pumpkin, belong to the family Cucurbitaceae. We review insights on their domestication from new phylogenies, archaeology and genomic studies. Ancestral state estimation on the most complete Cucurbitaceae phylogeny to date suggests that an annual life cycle may have contributed to domestication. Domestication started c. 11 000 years ago in the New World and Asia, and apparently more recently in Africa. Some cucurbit crops were domesticated only once, others multiple times (e.g. melon from different Asian and African populations). Most wild cucurbit fruits are bitter and nonpalatable to humans, and nonbitterness of the pulp apparently was a trait favoured early during domestication, with genomic data showing how bitterness loss was achieved convergently. The genetic pathways underlying lycopene accumulation, red or orange pulp colour, and fruit size and shape are only just beginning to be understood. The study of cucurbit domestication in recent years has benefitted from the increasing integration of archaeological and genomic data with insights from herbarium collections, the most efficient way to understand species’ natural geographic ranges and climate adaptations.

Contents
	Summary	1240
I.	Introduction	1240
II.	The diversity of cultivated Cucurbitaceae: traits of major and minor crops	1241
III.	Time and place of domestication	1245
IV.	The genomics of Cucurbitaceae domestication	1250
V.	Conclusions	1252
	Acknowledgements	1252
	References	1252

I. Introduction

The gradual transition from hunting and gathering to plant cultivation and animal husbandry began between the end of the Pleistocene and the beginning of the Holocene, some 12 000–10 000 years ago (Fuller et al., 2014; Arranz-Otaegui et al., 2018). The resulting sustainable nutrition of large sedentary populations represents one of the most significant transitions in the c. 300 000 year-long history of Homo sapiens (Larson et al., 2014; Richter et al., 2017). The reasons behind the implied behavioural changes in various human populations remain much debated, but are likely to have involved a combination of climate change, accompanying changes in the vegetation, prey animal densities, human demography, and human social systems (Belfer-Cohen & Goring-Morris, 2011; Larson et al., 2014). Eleven geographic regions have been identified as centres of plant and animal domestication in the New World, Africa, the Middle and Near East, Asia and New Guinea (Piperno, 2011; Fuller et al., 2014; Larson et al., 2014, and references therein).

Domestication involves humans acting as dispersers and modifiers of a crop's biotic and abiotic environment (Larson et al., 2014). It is a gradual process and often is not restricted to a single place or human population (reviewed in Meyer et al., 2012). As a result of this process, crop plants and domesticated animals share suites of modified traits referred to as the ‘domestication syndrome’, differentiating them from their wild ancestors (Darwin, 1868; De Candolle, 1884; Hammer, 1984; Pickersgill, 2007; Meyer et al., 2012; Stetter et al., 2017). In plants, the domestication syndrome often involves larger and more sugary fruits, reduction of physical and chemical defences in the parts used by humans, a change towards a more compact architecture, larger seeds, reduction in seed dormancy, larger inflorescences and non-shattering seeds (in grasses and legumes).

This review synthesises recent insights with older studies to produce a big picture of the domestication of Cucurbitaceae crops, highlighting different domestication trajectories as informed by phylogenetics, archaeology and genomics. The gourd family (Cucurbitaceae) has c. 1000 species, including numerous crops, such as cucumber (Cucumis sativus), bitter gourd (Momordica charantia), watermelon (Citrullus lanatus), preserving melon (Citrullus amarus), honey melon (Cucumis melo), squash and zucchini (Cucurbita pepo), and bottle gourd (Lagenaria siceraria) (Schaefer & Renner, 2011a,b; Renner & Schaefer, 2016; Fig. 1). Archaeobotanists have long documented the roles of cucurbits in ancient cultures based on remains of fruits, seeds and even leaves (e.g. Schweinfurth, 1883, 1884; Piperno, 2000, 2011; Wasylikowa & van der Veen, 2004), and old texts and illustrations document the spread of cucurbit crops from India or the Americas to the Mediterranean and northern Europe (Paris et al., 2012a,b,c, 2013; Paris, 2015). However, it is DNA sequencing of old and new material (usually leaf tissues), informed by meta-data from herbarium specimens, that has yielded the most surprising insights. Such work has by now identified closest relatives, ancestral areas and divergence times of pumpkin, zucchini, squashes, bottle gourd, bitter gourd, chayote, honey melon, watermelon, cucumber, bryonies, and sponge gourds (Sanjur et al., 2002; Erickson et al., 2005; Clarke et al., 2006; Renner et al., 2007; Volz & Renner, 2009; Schaefer & Renner, 2010b; Sebastian et al., 2010, 2012; Telford et al., 2011a,b; Filipowicz et al., 2014; Chomicki & Renner, 2015; Endl et al., 2018).

Details are in the caption following the image — **Figure 1**
Open in figure viewer PowerPoint

Cucurbitaceae crops and their wild progenitor to illustrate the domestication syndrome. (a, b) Honey melon (*Cucumis melo*). (a) Wild melon progenitor, Asian agrestis (*Cucumis melo* subsp. *melo* f. *agrestis*). (b) Domesticated melon (Asian lineage). (c, d) Watermelon (*Citrullus lanatus*). (c) Wild watermelon progenitor, Kordofan melon (*Citrullus lanatus* subsp. *cordophanus*). (d) Domesticated watermelon. (e, f) Cucumber (*Cucumis sativus*). (e) Wild cucumber progenitor (*C. sativus* f. *hardwickii*). (f) Domesticated cucumber. Photographs credited to: (a) Balkar Singh; (c) Harry Paris; (b, d, f) Creative commons; (e) Hanno Schaefer.

II. The diversity of cultivated Cucurbitaceae: traits of major and minor crops

Out of the c. 1000 species of Cucurbitaceae, 10 are of worldwide economic importance, cultivated globally, and are here considered ‘major crops’ (Table 1); another 23 are of more local commercial importance, are often cultivated in their native range, and might be called ‘minor crops’ (Table 2). The distribution of these 33 cultivated species over a phylogeny that samples 554 of the family's species and 95 of its 96 genera (Fig. 2) shows that the species used by humans are fairly clustered. All major crops are cultivated for their fruit, a particular type of berry called ‘pepo’ that is consumed ripe (e.g. pumpkin) or unripe (e.g. zucchini), raw (watermelon), cooked (squash), or pickled (gherkins). Cucurbita pepo is the only major crop also cultivated for its seeds and the oil pressed from them. Minor crops are cultivated for a wide range of purposes including raw fruits (e.g. Cucumis metuliferus), nutritious seeds (e.g. Citrullus mucosospermus) or to make oil (e.g. Telfairia occidentalis, T. pedata, Hodgsonia macrocarpa), cooked fruit (e.g. Trichosanthes cucumerina), sugary fruit used as a sweetener (Siraitia grosvenorii) or for their physical (Luffa aegyptiaca used as sponge) or medicinal properties (Citrullus colocynthis; Barghamdi et al., 2016).

Table 1. Traits and geographic origins of the major domesticated Cucurbitaceae crops.

Species	Common names	Area of origin	Area of domestication	Type of evidence for area of domestication	Timeline of domestication (years bp, minimum age)	Wild progenitor found?	Sister species	References
New World
Cucurbita argyrosperma	Silverseeded gourd	Mexico	Mexico	W, P	-	Yes (C. argyrosperma subsp. sororia)	C. moschata	Sanjur et al. (2002); Kates et al. (2017)
Cucurbita maxima	Pumpkins, Squashs	South America	Argentina	W, P	4000	Yes (C. maxima subsp. andreana)	C. ecuadorensis	Sanjur et al. (2002); Kates et al. (2017)
Cucurbita moschata	Butternut squash	Unknown	Unknown	-	-	No	C. argyrosperma	Sanjur et al. (2002); Kates et al. (2017)
Cucurbita pepo subsp. pepo	Summer squashs, zucchini, pumpkins	Mexico	Mexico	A, G, P, W	8000–10 000	No	C. okeechobeensis + C. lundelliana	Smith (1997); Sanjur et al. (2002); Kates et al. (2017)
Cucurbita pepo subsp. texana	Acorn, crookneck and pattypan squashes	Texas and nearby states	Texas	G, W	-	Yes	C. okeechobeensis + C. lundelliana	Sanjur et al. (2002); Kates et al. (2017)
Africa
Citrullus lanatus	Watermelon *Red and black seed melon (China)	Sudan (?)	Nile Valley *China (fleshy seed cultivar)	A, C, P, W? *C	5000 *400?	Yes, potentially	C. mucosospermus	Mote (1977); Wasylikowa & van der Veen (2004); Chomicki & Renner (2015); Renner et al. (2017, 2019)
Asia and Melanesia
Benincasa hispida	Wax gourd	Southeast Asia, Australasia	Southeast Asia, Indonesia?	A	2450 or before	Yes	B. fistulosa	Matthews (2003), Marr et al. (2007), Kocyan et al. (2007), Schaefer et al. (2009)
Cucumis melo subsp. melo	Numerous names for cultivars of Melon	India and Australia	Asia	A, G, P	2200	Yes	C. trigonus + C. picrocarpus	Walters (1989); Sebastian et al. (2010); Endl et al. (2018)
Cucumis sativus	Cucumber (Eurasian), pickling cucumber (East Asian), **Xishuangbanna cucumber	India	Asia, East Asia, **Xishuangbanna region	A, C, P, W	***2500	Yes (C. sativus var. hardwickii)	C. hystrix	Renner et al. (2007); Sebastian et al. (2010); Qi et al. (2013)
Lagenaria siceraria	Bottle gourd	Africa	Independently domesticated in Eurasia* and South America**	A, P	11 000 *10 000	Yes	L. breviflora	Kistler et al. (2014)
Momordica charantia	Bitter gourd	Africa	Africa or India, unclear	C, G	?	Yes	M. angolensis	Schaefer & Renner (2010a)

For the type of evidence for the domestication area; A, archaeological remains; C, other cultural evidence (e.g. linguistic or iconographic); G, genetic diversity of primitive landraces; P, phylogenetic evidence; W, inferred from wild progenitor distribution. ; (?) uncertainty remaining; ? unknown; *, ** and *** are used when crop species have been independently domesticated.

Table 2. Minor Cucurbitaceae crops.

Species	Tribe	Common names	Area of origin	Area of cultivation	Evidence for domestication	Habit	Sexual system	Timeline of cultivation (years bp, minimum age)	Use	References
Benincasa fistulosa	Benincaseae	Tinda	NW India (?)	India, Pakistan, E Africa	Yes	Annual	Monoecious		Fruit	Schaefer et al. (2009); Schaefer & Renner (2011b)
Citrullus amarus	Benincaseae	Preserving melon	South Africa, Namib desert	Mediterranean	Documented as crop in the Mediterranean region for > 1900 years	Perennial	Monoecious	>1900	Fruit rind boiled with sugar for jams	Bailey (1930); Chomicki & Renner (2015)
Citrullus colocynthis	Benincaseae	Colocynth	Northern Africa	Northern Africa, Middle East to India	No	Perennial	Monoecious	4000	Various medicinal uses from Ancient Egypt on	Renner et al. (2017)
Citrullus mucosospermus	Benincaseae	Egusi melon	West Africa	West Africa	No	Annual	Monoecious		Oil and protein rich seeds used for cooking	Achigan-Dako et al. (2015); Chomicki & Renner (2015); Renner et al. (2017)
Coccinia grandis	Benincaseae	Scarlet gourd, Kowai	East Africa	India and Southeast Asia	No	Perennial	Dioecious		Young shoots cooked and fruits	Holstein (2015)
Cucumis anguria	Benincaseae	Cackrey, Maroon cucumber, West Indian gherkin	Africa, naturalised in the New World	Tropical regions	Yes, nonbitter and smooth fruit	Perennial	Monoecious		Fruits pickled	Kirkbride (1993)
Cucumis melo subsp. meloides	Benincaseae	Tibish and Fadasi Melon	Africa, perhaps Nile valley	Sudan	Yes, nonbitter and larger fruit	Probably annual	Monoecious		Young fruits eaten cooked, seeds used in soups	Endl et al. (2018)
Cucumis metuliferus	Benincaseae	Kiwano	Sub-Saharan Africa	Worldwide	Yes, larger fruit and sweeter cultivars	Annual	Monoecious		Fruit eaten raw	Kirkbride (1993)
Cyclanthera pedata	Sicyoeae	Stuffing cucumber, caigua, achocha	Neotropics	South America	Yes, larger and smooth fruits	Perennial	Monoecious		Fruit cooked	Jeffrey (1980)
Hodgsonia macrocarpa	Sicyoeae	Lard fruit	Himalaya	China	No	Perennial	Monoecious		Seeds used to make oil or eaten roasted	Chien (1963)
Luffa acutangula	Sicyoeae	Sponge gourd, angled luffa	Arabian Peninsula, India	Tropical regions	Yes, larger fruit	Annual	Monoecious		Unripe fruit cooked, mature dried fruit used as a sponge	Filipowicz et al. (2014)
Luffa aegyptiaca	Sicyoeae	Sponge gourd	Southeast Asia	Tropical regions	Yes, larger fruit	Annual	Monoecious		Unripe fruit cooked, Mature dried fruit used as a sponge	Filipowicz et al. (2014)
Melothria mannii (syn. Cucumeropsis mannii)	Benincaseae	Egusi gourd	Central America	West Africa and Neotropics	No	Perennial	Monoecious		Seeds	Schaefer & Renner (2010b)
Melothria scabra	Benincaseae	Mouse melon, Mexican miniature watermelon,pepquinos	Mexico and Central America	Mexico and Central America	No	Perennial	Monoecious		Fruit eaten raw	Schaefer & Renner (2010b)
Momordia dioica	Momordiceae	Bristly balsa, pear, spiny gourd	South Asia	South Asia, especially India	No	Annual	Dioecious		Leaves as vegetable fruit boiled	Schaefer & Renner (2010a)
Momordica balsamina	Momordiceae	Balsam apple	Tropical Africa	Mediterranean?	No	Annual	Monoecious			Schaefer & Renner (2010a)
Momordica cochinchinensis	Momordiceae	Gac	Southeast Asia to North Australia	Southeast Asia	Yes, larger fruit	Perennial	Dioecious		Fruit eaten raw	Schaefer & Renner (2010a)
Sicana odorifera	Cucurbiteae	Cassabanana	South America	Latin America and Southern United States	No	Perennial	Monoecious		Fruit eaten raw	Schaefer & Renner (2011b)
Sicyos edulis (Sechium edule)	Sicyoeae	Chayote, christophine, chouchou	Mexico	Tropical regions	Yes, larger fruit, loss of bitterness and spines on fruits, increased sugar content	Perennial	Sicyos (Sechium) chinantlense	>500	Fruit eaten as vegetable	Newstrom (1991); Sebastian et al. (2012)
Siraitia grosvenorii	Siraitieae	Luo Han Guo	Southern China and Northern Thailand	China	No	Perennial	Dioecious		Fruit used as a low-calorie sweetener and in traditional Chinese medicine	Schaefer & Renner (2011b)
Telfairia occidentalis	Joliffieae	Fluted gourd, Fluted pumpkin	Tropical West Africa	Tropical West Africa	Yes, larger fruit	Perennial	Dioecious		Seeds used to make oil or roasted	Schaefer & Renner (2011b)
Telfairia pedata	Joliffieae	Oysternut, Zanzibar oil vine	Tropical East Africa	Tropical East Africa	No	Perennial	Dioecious		Seeds used to make oil or roasted	Schaefer & Renner (2011b)
Trichosanthes cucumerina	Sicyoeae	Snake gourd, Serpent gourd	Southeast Asia?	China	Yes, larger fruit	Annual	Monoecious	1000–800	Fruit cooked	Walters (1989)

This include species that are cultivated but not domesticated and species domesticated but only of local importance.

The domestication syndrome of Cucurbitaceae crops includes nonbitter fruits, increased fruit size, sometimes with higher sugar or carotenoid content, decreased physical defences (e.g. wild chayote fruits are spiny), and more compact and less branched growth with increased apical dominance. Selection of plants with desirable properties was probably begun by individual farmers and did not involve mass selection. All crop species went through population bottlenecks during domestication (Gross & Olsen, 2010). However, the number of rice plants sown by a household would be significantly higher than that of cucumber or squash plants, and the population size of founder plants in cucurbit domestication may therefore have been smaller than in Poaceae crops (Qi et al., 2013). Traits, such as nonbitter fruits, clearly were consciously selected for and were not a byproduct of selection for other features (see section IV.1 'Loss of bitterness').

Most Cucurbitaceae are annual or perennial herbs, and c. 50% of the species are monoecious, 50% dioecious (Kocyan et al., 2007; Schaefer & Renner, 2011b). Most major crop species (Table 1) are annuals with a monoecious sexual system in which every individual sets fruit. To test whether these traits were present already in the wild relatives of these crops or are overrepresented among domesticated forms, we performed a family-wide ancestral state estimation of life form evolution, scoring species as annual or perennial based on personal observations, labels of herbarium specimens and relevant literature. The results reveal that all but one of the major crop species are nested in lineages with an annual habit, while minor crops are either annual or perennial (Fig. 2). An annual life cycle may have facilitated domestication. Cucurbitaceae all have indeterminate growth, meaning that annual domesticated species are actually perennials that die at the end of the productive cycle due to the exhaustion of the vegetative organs imposed by the selection for high productivity or due to unfavourable climate conditions outside their centre of origin. In other words, perennial Cucurbitaceae crops are cultivated as annuals, but this is a management practice, not the result of genetic changes. Perennial wild species often build up large underground tubers from which annual shoots emerge (Schaefer & Renner, 2011b) that flower in their first year (H. Schaefer, pers. obs.).

Most Cucurbitaceae have unisexual flowers, and based on outgroup comparison, dioecy appears to be the ancestral state in the family (Zhang et al., 2006). There have been numerous evolutionary changes between monoecy and dioecy (Volz & Renner, 2008; Schaefer & Renner, 2010b), and the sexual systems of many wild species are neither reliably known nor can be extrapolated from herbarium material, especially in climbers in which male and female flowers appear distant from each other and at different times. Some cucurbit climbers, such as species of Gurania and Psiguria, only bear male flowers until they reach sunny conditions (in the canopy or because of a disturbance) and then form female flowers (Condon & Gilbert, 1988). In many dioecious species, prolonged careful observations of numerous individuals also reveal ‘leaky dioecy’, the occasional development of flowers of both sexes in dioecious individuals (Schaefer & Renner, 2010b).

III. Time and place of domestication

1. The New World as a centre of cucurbit domestication

Several important Cucurbitaceae crop species were domesticated in the New World in pre-Columbian times (Larson et al., 2014). The most prominent are the globally important squashes and pumpkins (Cucurbita spp.; Table 1; Fig. 3). The genus Cucurbita had a wide pre-Holocene distribution and was adapted to the disturbed habitats maintained by large-bodied mammals that also dispersed the bitter fruits, potentially because these mammals had few bitter taste receptor genes (Kistler et al., 2015). Population fragmentation inferred from plastid genomes suggests that the Holocene megafaunal extinction led to a decline in wild Cucurbita, which were then ‘rescued’ by anthropogenic dispersal during domestication (Kistler et al., 2015). Archaeological evidence points to northern South America and Central America as places of the earliest pumpkin domestication, c. 10 000 years ago (Smith, 1997).

Of the four major crop species in the genus Cucurbita, C. pepo is native to North America (Northeast Mexico, and the Southeast and Central United States; Bailey, 1943; Paris et al., 2012c), and archaeological remains suggest an initial domestication some 8000–10 000 yr ago in Mexico (Smith, 1997). Independent domestication occurred in Eastern North America (Sanjur et al., 2002). These two domestication events led to the forms now classified as C. pepo subsp. pepo and C. pepo subsp. ovifera (Paris et al., 2012c; Table 1; Fig. 3). No wild populations of subsp. pepo have been found, but wild populations of subsp. ovifera occur in Texas and nearby states, and a 3^rd taxon (C. pepo subsp. fraterna) occurs in Northeast Mexico (Nee, 1990). However, C. pepo subsp. ovifera is not monophyletic, instead appearing in at least two places in a nuclear phylogeny, with a mix of domesticated and nondomesticated forms, suggesting either introgression, multiple domestication centres and/or broad domestication bottlenecks (incomplete lineage sorting in the crop) (Kates et al., 2017; our Fig. 3). American cultivars of C. pepo subsp. pepo reached Italy in the 16^th century, where in the mid-19^th century they gave rise to the cultivar group known as zucchini. From Italy, zucchini returned to the Americas, and today, they are one of the most widely cultivated crops of the family (Lust & Paris, 2016).

The second domesticated species of Cucurbita is C. maxima, with the subspecies maxima (Hubbard squash, buttercup squash, giant pumpkin) and andreana. The former was cultivated as early as 4000 bp along the coast of Peru where it may have been domesticated, but apparently never left the Neotropics during pre-Columbian times (Sauer, 1993; Piperno & Stothert, 2003). The other subspecies, andreana, appears to have been domesticated in what is today Argentina (Nee, 1990; Sanjur et al., 2002; Kates et al., 2017).

The third domesticated species of Cucurbita, C. moschata – the butternut squash – may have originated in Northern South America (Sanjur et al., 2002), consistent with high landrace diversity, and commonness of landraces with primitive traits such as small dark seeds, lignified, warty rind and bitter pulp (Nee, 1990). However, nuclear sequence data cast doubt on a South American origin of this species (Kates et al., 2017).

The fourth domesticated species of Cucurbita, C. argyrosperma is native to Mexico (Sanjur et al., 2002; Kates et al., 2017) and probably was domesticated there, although the timeline of its domestication remains unclear because of a lack of archaeological remains.

Another Cucurbitaceae crop from a different genus domesticated in the New World is Sicyos edulis, the chayote. Linguistic data, together with cultivar genetic diversity, pinpoint Mexico as its centre of domestication (Newstrom, 1991), consistent with a biogeographic analysis showing Mexico as the ancestral area of the clade containing chayote (Sebastian et al., 2012). Hernandez (1550) documented the use of the chayote by the Aztecs. It became a worldwide crop in tropical, subtropical and warm temperate regions in the 19^th century when it was introduced in Africa, Southern Europe, Asia and the West Indies, with the precise dates of introduction known in most cases (Newstrom, 1991). A potential wild progenitor population of chayote has been found in Mexico, with small, spiny and bitter fruits, but some less bitter and containing sugar (Newstrom, 1991).

Melothria mannii is a minor crop (Table 2) cultivated for its nutritious seeds as a so-called ‘egusi-crop’ (for making stews) in both West Africa and Central and South America. Biogeographic reconstruction indicates that it is native to America (Schaefer & Renner, 2010a; treating the species under the erroneous name Melothria sphaerocarpa). Whether it has been domesticated independently in America and Africa is unclear. It could have been brought to Africa as a domesticate during the slave trade, but natural transatlantic dispersal of either wild or cultivated forms cannot be excluded (Schaefer & Renner, 2010a).

2. Africa as a centre of cucurbit domestication

The genus Citrullus is the most economically important Cucurbitaceae lineage in Africa where it has seven species (Chomicki & Renner, 2015) of which several are cultivated and some are used as bush food (C. amarus, C. naudinianus). The taxonomy of the genus Citrullus until recently contained misapplications of names, including that of the watermelon, C. lanatus, itself (Renner et al., 2014; Chomicki & Renner, 2015). The erroneous nomenclature led to a number of confusions, including the reference to ‘wild’, ‘semi-wild’ and ‘domesticated’ populations of watermelon that are in fact distinct species ‘separated’ by undoubted wild species. Citrullus lanatus is the most economically important species in the genus. It was long thought to originate from South Africa because of a taxonomic mistake involving the oldest collection of a wild South African species described by a student of Linnaeus, which in the 1930s was wrongly synonymised with the cultivated watermelon (Bailey, 1930). Phylogenetic evidence, including DNA from the original specimen collected near Cape Town in 1773 by Linnaeus's student Carl Peter Thunberg, showed that no South African material is closely related to the domesticated watermelon. The earliest archaeological evidence of cultivated watermelon consists of seeds dated to c. 5000 bp (8000? bp) from Wan Muhuggiag in Libya (Wasylikowa & van der Veen, 2004). An oblong, large fruit served on a tray and with the characteristic striped fruit skin of watermelon is shown on a wall painting in a Pharaonic tomb from Meir, Northwest of Asyut (reproduced in Paris, 2015), suggesting that the fruit was eaten raw, which would indicate the availability of sweet, nonbitter watermelons in Egypt 4000 years ago (Chomicki & Renner, 2015).

Four hypotheses have been proposed for the origin of the watermelon: First, that it descends from the northern African colocynth (C. colocynthis; Singh, 1978; Sain et al., 2002; McCreight et al., 2013). Second, that it derives from the South African citron melon, C. amarus (Robinson & Decker-Walters, 1997; Maynard & Maynard, 2000; Rubatsky, 2001). Third, that it stems from the West African C. mucosospermus (Guo et al., 2013; Chomicki & Renner, 2015), and fourth, that it both originated from and was domesticated in Northeastern Africa (Paris, 2015). A phylogenetic analysis of Citrullus (Chomicki & Renner, 2015), together with genetic, archaeological and historical data (reviewed by Paris, 2015) rejects the first two hypotheses, leaving West Africa and Northeast Africa. Phylogenomic analyses of nuclear gene sequences suggested that the white-fleshed Sudanese Kordophan melon is the closest relative of the domesticated watermelon (Renner et al., 2019; Fig. 4). The lack of bitterness and high sugar content of Kordophan melons (Ter-Avanesyn, 1966), however, leaves open the possibility that these melons represent a landrace. Phylogenomic data also imply that the West African egusi melon, C. mucosospermus, bred for its nutritious seeds (Achigan-Dako et al., 2015), was domesticated from a different gene pool than that of the watermelon.

Another crop in the genus Citrullus is the preserving melon, C. amarus, which originates from Southern Africa (Chomicki & Renner, 2015; Renner et al., 2017 provide a distribution map). This species, referred to as ‘citron melon’ in its wild South African form, is an important crop in the Mediterranean region where the ripe fruit, including its rind, is boiled with sugar to make jams (Laghetti & Hammer, 2007). It is also used in specialty baking, for example, in fruit cake mixes and Christmas baking in Mexico and the United States (Bush, 1978). The species was introduced into the Mediterranean region from at least the Roman era, as evidenced by mention in a Latin cookbook (De Re Coquinaria, ad 77–516) as citrium (Paris, 2015), and there is archaeological and iconographic evidence that it was a widely used crop all around the Mediterranean and Europe from at least the 14^th century (Paris et al., 2013; Paris, 2015). The species was also introduced to Australia by Afghan cameleers in the mid 1800s to early 1900s, who used its fruits as a feed source for their camels; it is now a weed of summer fallows in Australia (Shaik et al., 2017).

The colocynth, C. colocynthis, has also been cultivated since Ancient Egyptian times as a medicinal plant and a source of oil but has not been domesticated. Colocynth seeds are found from 5000 bp (8000 bp) onwards in archaeological sites in Libya, Egypt and the Near East (Wasylikowa & van der Veen, 2004), and the species may have reached India and Pakistan by human transport.

3. Asia and Melanesia as centres of cucurbit domestication

The most important Cucurbitaceae crop from Asia is the cucumber, Cucumis sativus. Cucumbers have been domesticated from wild Indian C. sativus var. hardwickii (Qi et al., 2013), which has small bitter-tasting or sour fruits that are ellipsoid or subglobose and 5–8 cm long (Fig. 1e); it is known from India and Northwest and West Thailand, growing wild and sold in local markets. Three main cultivar groups of cucumber were subsequently selected for distinct purposes, namely Eurasian cucumbers (our slicing cucumbers eaten raw and immature), East Asian cucumbers (pickling cucumbers) and Xishuangbanna cucumbers (Fig. 5, inset). Based on demographic modelling, the East Asian C. sativus cultivars diverged from the Indian cultivars c. 2500 years ago, that is close to a Chinese text reporting the introduction of cucumber to China during the Han dynasty (Qi et al., 2013). The Xishuangbanna cultivar (C. sativus var. xishuangbannanensis) was selected for high β-carotene content in the mature pulp; its fruits are eaten boiled or raw during different stages of maturity (Yang et al., 1991; Renner, 2017).

Honey melon (Cucumis melo) was domesticated at least once in Asia and once in Africa (Endl et al., 2018; Fig. 5). The oldest melon remains from Asia date to 3000 bc in China (Watson, 1969) and to 2300–1600 bc in the Indus valley (Vishnu-Mittre, 1974). The oldest African melon seeds date to a site from 3700 to 3500 bc in Lower Egypt (van Zeist & de Roller, 1993; El Hadidi et al., 1996). The honey melon cultivars grown today can be traced back to two wild lineages that are estimated to have diverged 1–3 Ma. The first one is restricted to Asia (C. melo subsp. melo), while the second, C. melo subsp. meloides Endl & H. Schaef., is widespread throughout Africa. The Asian lineage gave rise to all modern cultivars including the commercially important ‘Galia’, ‘Cantaloupe’, and ‘Yellow Honeydew’ melons, while the African lineage gave rise to the ‘Tibish’ and ‘Fadasi’ melons, landraces still grown in the Sudanese region but gradually being replaced by imported cultivars from Asia. A third wild C. melo lineage is restricted to Australia and New Guinea but apparently was never domesticated (Endl et al., 2018). The C. melo clade is sister to a long overlooked Indian perennial, C. trigonus and the Australian C. picrocarpus (Endl et al., 2018).

Lagenaria siceraria, the bottle gourd, the dry empty fruits of which are used as watertight containers, is native to Africa (Table 1). The species appears to have been cultivated as early as 11 000 years ago in Asia and independently in the Americas, where it was widespread 8000 bp (Erickson et al., 2005; Kistler et al., 2014). For Polynesia, genetic data suggest arrivals from both Asia and South America, after the species had become a well established crop in those regions (Clarke et al., 2006). An older scenario suggested that the bottle gourd was brought to the New World by Paleoindians as they colonised the continent (Erickson et al., 2005), but this would imply that a tropical plant could have been planted and harvested under Arctic climate conditions. A more recent phylogenetic analysis of a denser sample of archaeological wild and cultivated American and Asian bottle gourds indicated that the species was brought from Africa to Eurasia by humans, but reached America by natural transoceanic dispersal from Africa before the arrival of humans there (Kistler et al., 2014). Strangely, archaeological evidence for early bottle gourd cultivation is restricted to the Pacific coast of South America, which does not match the species’ presumed transoceanic arrival from Africa. Bottle gourd used to be an important vegetable in Europe, later replaced by zucchini (Lust & Paris, 2016).

The bitter gourd, Momordica charantia, another major cucurbit crop (Table 1), is native to Africa (Schaefer & Renner, 2010b) and Madagascar, but today is most extensively used in Asian cuisines. Its use in Kerala (Southern India) is documented from the 17^th century onwards (Rheede, 1688; Marr et al., 2004). It remains unclear where this important crop was domesticated, and more sampling of landraces and wild forms from Madagascar, mainland Africa and Southern India is necessary to confirm its region of domestication.

The wax gourd, Benincasa hispida, is documented from an archaeological site in Thailand dated from 9980 to 9530 bp (Pyramarn, 1989), and in New Guinea, rind and seeds have been found at the Kuk swamp archaeological site (Golson et al., 2017) dated to 2450 bp (Matthews, 2003). Seed size does not resolve the status of these archaeological finds as cultivated or wild because at least the size of the New Guinean seeds is within the range of domesticates (Marr et al., 2007). The related minor crop Tinda or Indian round gourd, Benincasa fistulosa (syn. Praecitrullus fistulosus), is cultivated in India and Pakistan and at a very small scale in East Africa, where it has been introduced. Its origin and area of domestication are unclear but wild forms exist in Northwest India (Renner & Pandey, 2013).

The area of domestication of the sponge gourd, Luffa aegyptiaca, which occurs throughout Southeast Asia, is unknown and the entire genus with eight species worldwide is surprisingly poorly understood (Marr et al., 2005; Filipowicz et al., 2014). Small-fruited wild forms occur in Australia and Indonesia (Marr et al., 2005). Wild forms of the angled loofah, L. acutangula, are known from the Arab Peninsula and India (Filipowicz et al., 2014). Interestingly, none of the three Neotropical Luffa species has been domesticated.

IV The genomics of Cucurbitaceae domestication

So far, 11 reference genomes of cucurbits have been produced, namely C. sativus var. sativus cv 9930 and cv Gy14, one wild cucumber (C. sativus var. hardwickii PI 183967), one cultivated melon (C. melo cv DHL92), two cultivated watermelons (C. lanatus subsp. vulgaris cv 97103 and cv Charleston Gray), four cultivated Cucurbita species (C. maxima cv Rimu, C. moschata cv Rifu, C. pepo cv MU-CU-16, and C. argyrosperma), and one cultivated bottle gourd (Lagenaria siceraria cv USVL1VR-Ls) (Huang et al., 2009b; Garcia-Mas et al., 2012; Guo et al., 2013; Qi et al., 2013; Sun et al., 2017; Wu et al., 2017; Wang et al., 2018; Montero-Pau et al., 2018; Ruggieri et al., 2018; Barrera-Redondo et al., 2019), and the number is rapidly increasing. Zheng et al. (2019) summarised the genomic resources available by 2018. Comparisons of nondomesticated wild forms with domesticated accessions imply that domestication of cucurbit fruits always first required loss of fruit bitterness, a trait conferred by toxic cucurbitacins (Zhou et al., 2016). Selection also affected the seed coat, carotenoid content and sugar content. Below we summarise how this may have occurred. We restrict our review of comparative and functional genomics of cucurbit crop traits to traits directly relevant to domestication. Molecular mechanisms underlying flower sex-determination, fruit development, and spine development in cucumber are reviewed by Che & Zhang (2019).

1. Loss of bitterness

Some wild cucurbit species have sweet fruit pulp, and some of these are minor crops (Cucumis anguria, Cucumis metuliferus, Melothria scabra); others are bush food collected from the wild and eaten by kids, such as the fruit pulp of wild Kedrostis foetidissima, Momordica species, Solena heterophylla, and some Trichosanthes (e.g. Murthy et al., 2013). Most wild cucurbits, however, have bitter fruits, with bitterness conferred by a group of terpenoid compounds called cucurbitacins. Cucurbitacins are very effective in direct plant defence against herbivores and are present in leaves, roots and fruits in many nondomesticated cucurbits. With the exception of the bitter gourd (Momordica charantia), for which some cultivars are very bitter when it is harvested, Cucurbitaceae fruit crops have lost bitterness during domestication. Nonbitter remains of the squash Cucurbita moschata that date to 9200 bp indicated that automatic selection (sensu Harlan et al., 1973) for nonbitter fruits occurred very early (Piperno & Dillehay, 2008).

The Bi gene confers bitterness to the whole plant (Huang et al., 2009 and references therein), and a genetic and biochemical study showed that Bi encodes a cucurbitadienol synthase that catalyses the first committed step in cucurbitacin C biosynthesis in cucumber (Shang et al., 2014). Two bHLH transcription factors regulate cucurbitacin C biosynthesis by upregulating Bi in the leaves (Bl) and fruits (Bt) directly via binding in the E-box elements of the Bi promoter (Shang et al., 2014). In cucumber, no selective sweep was associated with the Bi gene (Qi et al., 2013), suggesting that loss of cucurbitacin biosynthesis in the whole plant would have been deleterious, even in cultivated crops (notably in terms of defence against generalist herbivores). Examination of different cucumber lines with varying bitterness has revealed that domestication of nonbitter cucumber occurred via the downregulation of Bt, either by mutation in its cis-acting elements or by affecting the binding site (Qi et al., 2013; Shang et al., 2014; Zhou et al., 2016). A genomic analysis of homologues comparing cucumber, melon and watermelon (producing cucurbitacin C, B and E, respectively) revealed a convergent domestication sweep at the Bt loci and the loss of bitterness is, in all cases, due to convergent mutations at this locus (Shang et al., 2014; Zhou et al., 2016). Selected mutations in an upstream regulatory gene controlling the expression of a given pathway in specific tissue may be common during domestication, as this can help avoid pleiotropic effects associated with modification of the pathway itself (Lenser & Theißen, 2013).

2. Selection for sweetness

For several Cucurbitaceae crop species, especially watermelon (Citrullus lanatus) and honey melon (Cucumis melo), selection for sweet fruits has occurred during domestication. Genome analysis and transcriptomics in the watermelon revealed that α-galactosidase, insoluble acid invertase, neutral invertase, sucrose phosphate synthase, UDP-glucose 4-epimerase, soluble acid invertase and UDP-galactose/glucose pyrophosphorylase are the main enzymes that regulate sugar unloading and metabolism during ripening (Guo et al., 2013). In total, 62 sugar metabolism genes and 76 sugar transporter genes have been annotated, with 13 and 14, respectively, differentially expressed in fruit flesh (Guo et al., 2013). In honey melon, 63 genes involved in sugar metabolism have been annotated (Garcia-Mas et al., 2012). Of the sugar transporters found in domesticated (sweet and red-fleshed) watermelon, but not in citron melons (Citrullus amarus (PI296341-FR)), two SWEET-like sugar transporters (Sugars Will Eventually be Exported Transporter (SWEET)) were highly expressed in developing red-flesh of watermelon (but not rind), and their expression level was correlated to the amount of fruit sugar, suggesting that they increase fruit flesh sweetness by facilitating the active transmembrane transport of sugars (Guo et al., 2015).

Work on watermelon has further identified a tonoplast sugar transporter (ClTST2) that pumps sucrose, glucose and fructose inside the fruit's vacuoles (Ren et al., 2018). Cross-comparisons across hundreds of Citrullus accessions spanning several species revealed that increased expression of ClTST2 was a major event in the domestication of the watermelon. ClTST2 is regulated by a sugar-induced transcription factor called SUSIWM1, and a single SNP in the tonoplast sugar transporter (ClTST2) has been fixed in the sweet, domesticated watermelon, and underlies a sugar accumulation quantitative trait locus (QTL) in watermelon (Ren et al., 2018). Therefore, it appears that increased ClTST2 expression by enhanced binding efficiency of SUSIWM1 to the ClTST2 promoter was a key event increasing sugar content during the domestication of the watermelon.

Altogether these data for honey melon and watermelon suggest that increased sugar content resulted from selection on dozens of genes altering sugar metabolism or transport.

3. Selection for larger fruits

In all 10 major Cucurbitaceae crops (Table 1), humans selected for larger fruits. Fruit size is essentially controlled by three processes in the ovary: cell differentiation (e.g. the definition of the number of carpels), cell division and cell expansion. Carpel number only varies from three to seven, with even very large specimens of Cucurbita maxima only having five to seven carpels (Grumet & Colle, 2017). The increase in fruit size therefore mostly involves shifts in the regulation of cell division and in cell expansion. The transcriptional master regulators of the fruit size gene networks are still unclear, but so far phytohormone-related genes (auxin, cytokinins and gibberelins), microtubule-related genes and cyclin-related genes appear to be the key players controlling fruit size.

In watermelon, Citrullus lanatus, two MADS box genes similar to the tomato ripening and expansion gene TAGL1 have been characterised and are highly expressed during fruit expansion and ripening, suggesting that they regulate both processes (Guo et al., 2013). In cucumber, C. sativus, analysis of QTL identified a single selective sweep with 19 genes, one of which encodes a cyclin involved in cell proliferation (Qi et al., 2013). Another study identified 12 QTLs for fruit size in this species that were linked to different aspects of size, in particular length and width (Weng et al., 2015), and that have been selected in different ways in the three domestication directions of Cucumis sativus (Fig. 5 inset). Transcriptome analysis of cucumber revealed thousands of differentially expressed genes, including many linked to microtubules and cyclins (cell division) (Jiang et al., 2015). A single recessive gene, spontaneous short fruit 1 (sf1), appears to regulate cucumber length through auxin and cytokinin signalling (Wang et al., 2017).

Clearly the regulation of fruit size is a complex process, and domestication has affected it in different ways (for instance, long and thin Eurasian salad cucumbers vs short and thick East Asian pickling cucumbers; Fig. 5), implying changes in the spatio-temporal fine-tuning of genes controlling cell division and expansion. The world's largest fruits are produced by Cucurbita maxima cv Dill's Atlantic Giant, with record fruits weighing > 1000 kg. Despite the huge variation in fruit size and weight in Cucurbitaceae crops and their close relatives, the regulatory control underpinning these changes is not well understood. Functional characterisation of candidate genes regulating cell division and expansion in fruits is an exciting future research path. This approach would pave the way for interesting comparisons of fleshy fruit development across angiosperms of which the mechanisms are currently almost exclusively known in tomato (Karlova et al., 2014).

4. Seed traits

Relatively few Cucurbitaceae crops are cultivated for their seeds. Most important economically are pumpkin seeds (Cucurbita pepo). The Styrian pumpkin, C. pepo subsp. pepo var. styriaca, is a variety that lost the seed testa following a single natural mutation in the 19^th century (Teppner, 2004). Another cucurbit cultivated for its seeds is the West African egusi melon, C. mucosospermus, which has high nucleotide divergence from the domesticated watermelon (C. lanatus) in loci controlling fatty acid metabolism in seeds (Guo et al., 2013), consistent with the egusi melon's role as a seed crop. Mendelian genetics identified that a single recessive locus controlled the egusi seed type in Citrullus (Gusmini et al., 2004). In China, a form of watermelon with fleshy reddish seeds is grown for its seeds, which are toasted and eaten as a snack, and apparently this use dates to ad 1250 (Mote, 1977).

5. Selection for high carotenoid content

Several cucurbit crops accumulate β-carotene or lycopene, antioxidants that are highly beneficial to human health. Orange or red fruit pulp due to naturally high carotenoid concentrations are also found in wild species, for instance in the genera Momordica, Solena and Trichosanthes. Studies of crops have focused on watermelon and honey melon, in which the carotenoid accumulation results from the regulation of several metabolic genes (Garcia-Mas et al., 2012; Guo et al., 2013). In domesticated red-flesh watermelons, two key genes of the carotenoid biosynthetic pathway – phytoene synthase (PSY) and phytoene desaturase (PDS) – are upregulated during fruit development (Guo et al., 2011, 2015).

Lycopene accumulation in watermelon has been linked to 19 transcription factors, with the accumulation mirrored by low expression of lycopene cyclase, the enzyme that converts lycopene into β-carotene (Grassi et al., 2013). Another lycopene-rich cucurbit is the Xishuangbanna cucumber (Cucumis sativus var. xishuangbannanensis, Renner, 2017), a form of cucumber domesticated c. 2500 years ago by the Hani ethnic group in China, Laos and Vietnam, with high sugar and β-carotene content, similar to that of a melon. Its orange flesh is due to a substitution of alanine to asparagine at position 257 of the BCH1 gene, encoding a β-carotene hydroxylase (Qi et al., 2013). This mutation leads to a nonfunctional β-carotene hydroxylase that cannot convert β-carotene into zeaxanthin, leading to an accumulation of β-carotene (Qi et al., 2013).

Building on these results, Zhang et al. (2017) reported that high expression of a chromoplast-localised phosphate transporter (ClPHT4;2) is needed for lycopene accumulation. While ClPHT4;2 is present in both domesticated red-fleshed watermelon and white-fleshed close relatives, it is expressed at a very low level in white-fleshed watermelons. High expression of ClPHT4;2 relates to the presence of key cis-acting elements in its promoters that enables binding of sugar, abscisic acid and ethylene inducible transcription factors ClbZIP1 and ClbZIP2. These cis-acting elements are lacking in white-fleshed Citrullus (Zhang et al., 2017). That ClbZIP1 and ClbZIP2 are sugar-inducible led Zhang et al. (2017) to suggest that selection for sweetness and red colour occurred concurrently in the watermelon. However, the fruits of Citrullus lanatus subsp. cordophanus have white flesh combined with a high sugar content (Ter-Avanesyn, 1966).

V. Conclusions

We have highlighted the current state of research on Cucurbitaceae domestication, discussing both major and minor crops. Major crop species arose from annual and monoecious lineages within four of the 15 phylogenetically supported tribes of the family (Table 1), and were domesticated in North, Central and South America, Northeastern Africa, East, Southern, and Southeastern Asia, and on the island of New Guinea, in some cases overlapping with well known centres of plant and animal domestication. In many cases, the first trait selected on by man likely was nonbitterness of pulp, and comparative genomic analyses have revealed that, in cucumber, honey melon and watermelon, loss of fruit bitterness results from convergent domestication sweeps involving mutations at the Bt locus (Shang et al., 2014; Zhou et al., 2016). Both honey melon and watermelon were domesticated in Northeast Africa, perhaps in the Upper Nile region of what is now Sudan, but honey melon was also domesticated independently in Asia. Only a tiny subset of all flowering plants has been brought into cultivation with certain traits, such as an herbaceous habit or the ability to grow in disturbed anthropogenic environments, apparently key reasons. For Cucurbitaceae, monoecy combined with an annual life cycle appears to have been a factor (Fig. 1). Our review also highlights how the study of crop domestication needs to combine genomic efforts with traditional systematics and herbarium-verified specimens; this approach is the most efficient way to infer species’ geographic distributions and likely climatic adaptations.

Deciphering the domestication history of the major Cucurbitaceae crops will require further integration of population genomics with collection-based research and archaeological samples. The huge array of useful traits and the large genetic diversity found in the 23 minor cucurbit crops, as well as in wild progenitor populations of major crops, opens up a number of exciting avenues for de novo domestication, using CRISPR–Cas9 genome editing (Zsögön et al., 2018). This approach would be especially useful for plants like the watermelon, in which disease-resistance genes have been lost during domestication (Guo et al., 2013).

Acknowledgements

We thank three reviewers for their comments, and Harry Paris, Shaogui Guo and Bob Jarrett for discussion, and Oscar Alejandro Pérez-Escobar for generating the phylogeny shown in Fig. 4. Financial support came from the DFG (grants RE 603/27-1 and SCHA 1875/4-1) and the Elfriede and Franz Jakob Foundation for research at the Botanical Garden Munich, Germany. GC is supported by a Glasstone Research Fellowship and a Junior Research Fellowship at Queen's College, University of Oxford, UK.

References

Achigan-Dako EG, Avohou ES, Linsoussi C, Ahanchede A, Vodouhe RS, Blattner FR. 2015. Phenetic characterization of Citrullus spp. (Cucurbitaceae) and differentiation of egusi-type (C. mucosospermus). Genetic Resources and Crop Evolution 62: 1159–1179.
Arranz-Otaegui A, Carretero LG, Ramsey MN, Fuller DQ, Richter T. 2018. Archaeobotanical evidence reveals the origins of bread 14,400 years ago in northeastern, Jordan. Proceedings of the National Academy of Sciences, USA 115: 7925–7930.
Bailey LH. 1930. Three discussions in Cucurbitaceae. Gentes Herbarum 2: 175–186.
Bailey LH. 1943. Species of CucurbitaGentes Herbarum 6: 266–322.
Barghamdi B, Ghorat F, Asadollahi K, Sayehmiri K, Peyghambari R, Abangah G. 2016. Therapeutic effects of Citrullus colocynthis fruit in patients with type II diabetes: a clinical trial study. Journal of Pharmacy & Bioallied Sciences 8: 130–134.
Barrera-Redondo J, Ibarra-Laclette E, Vázquez-Lobo A, Gutiérrez-Guerrero YT, de la Vega GS, Piñero D, Montes-Hernández S, Lira-Saade R, Eguiarte LE. 2019. The genome of Cucurbita argyrosperma (Silver-Seed Gourd) reveals faster rates of protein-coding gene and long noncoding RNA turnover and neofunctionalization within Cucurbita. Molecular Plant 12: 506–520.
Belfer-Cohen A, Goring-Morris AN. 2011. Becoming farmers. Current Anthropology 52: S209–S220.
Bush A. 1978. Citron melon for cash and condiment. Economic Botany 32: 182–184.
Che G, Zhang X. 2019. Molecular basis of cucumber fruit domestication. Current Opinion in Plant Biology 47: 38–46.
Chien H. 1963. “Lard fruit” domesticated in China. Euphytica 12: 261–262.
Chomicki G, Renner SS. 2015. Watermelon origin solved with molecular phylogenetics including Linnaean material: another example of museomics. New Phytologist 205: 526–532.
Clarke AC, Burtenshaw MK, McLenachan PA, Erickson DL, Penny D. 2006. Reconstructing the origins and dispersal of the Polynesian bottle gourd (Lagenaria siceraria). Molecular Biology and Evolution 23: 893–900.
Condon MA, Gilbert LE. 1988. Sex expression of Gurania and Psiguria (Cucurbitaceae): neotropical vines that change sex. American Journal of Botany 75: 875–884.
Darwin C. 1868. Variation of plants and animals under domestication. London, UK: John Murray.
De Candolle A. 1884. Origin of cultivated plants. London, UK: Kegan Paul, Trench & Co.
El Hadidi MN, Fahmy AG, Willerding U. 1996. The paleoethnobotany of locality 11c, Hierakonpolis (3880–3500 BC), Egypt 1. Cultivated crops and wild plants of potential value. Taekholmia 16: 31–44.
Endl J, Achigan-Dako EG, Pandey AK, Monforte AJ, Picó B, Schaefer H. 2018. Repeated domestication of melon (Cucumis melo) in Africa and Asia and a new close relative from India. American Journal of Botany 105: 1662–1671.
Erickson DL, Smith BD, Clarke AC, Sandweiss DH, Tuross N. 2005. An Asian origin for a 10,000-year-old domesticated plant in the Americas. Proceedings of the National Academy of Sciences, USA 102: 18315–18320.
Filipowicz N, Schaefer H, Renner SS. 2014. Revisiting Luffa (Cucurbitaceae) 25 years after C. Heiser: species boundaries and application of names tested with plastid and nuclear DNA sequences. Systematic Botany 39: 205–215.
Fuller DQ, Denham T, Arroyo-Kalin M, Lucas L, Stevens CJ, Qin L, Allaby RG, Purugganan MD. 2014. Convergent evolution and parallelism in plant domestication revealed by an expanding archaeological record. Proceedings of the National Academy of Sciences, USA 111: 6147–6152.
Garcia-Mas J, Benjak A, Sanseverino W, Bourgeois M, Mir G, González VM, Hénaff E, Câmara F, Cozzuto L, Lowy E et al. 2012. The genome of melon (Cucumis melo L.). Proceedings of the National Academy of Sciences, USA 109: 11872–11877.
J Golson, TP Denham, PJ Hughes, P Swadling, J Muke, eds. 2017. Ten thousand years of cultivation at Kuk swamp in the highlands of Papua New Guinea. Terra Australis 46. Canberra, ACT, Australia: ANU Press.
Grassi S, Piro G, Lee JM, Zheng Y, Fei Z, Dalessandro G, Giovannoni JJ, Lenucci MS. 2013. Comparative genomics reveals candidate carotenoid pathway regulators of ripening watermelon fruit. BMC Genomics 14: 781.
Gross BL, Olsen KM. 2010. Genetic perspectives on crop domestication. Trends in Plant Science 15: 529–537.
Grumet R, Colle M. 2017. Genomic analysis of cucurbit fruit growth. In: R Grumet, N Katzir, J Garcia-Mas, eds. Genetics and genomics of Cucurbitaceae. Cham, Switzerland: Springer International, 321–344.
Guo S, Liu J, Zheng Y, Huang M, Zhang H, Gong G, He H, Ren Y, Zhong S, Fei Z et al. 2011. Characterization of transcriptome dynamics during watermelon fruit development: sequencing, assembly, annotation and gene expression profiles. BMC Genomics 12: 454.
Guo S, Sun H, Zhang H, Liu J, Ren Y, Gong G, Jiao C, Zheng Y, Yang W, Fei Z et al. 2015. Comparative transcriptome analysis of cultivated and wild watermelon during fruit development. PLoS ONE 10: e0130267.
Guo S, Zhang J, Sun H, Salse J, Lucas WJ, Zhang H, Zheng Y, Mao L, Ren Y, Wang Z et al. 2013. The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nature Genetics 45: 51–58.
Gusmini G, Wehner TC, Jarret RL. 2004. Inheritance of egusi seed type in watermelon. Journal of Heredity 95: 268–270.
Hammer K. 1984. Das Domestikationssyndrom. Kulturpflanze 32: 11–34.
Harlan JR, De Wet JMJ, Price EG. 1973. Comparative evolution of cereals. Evolution 27: 311–325.
Hernandez F. 1550. Historia de las plantas de Nueva Españia. Vol. III. Books 5,6,7:699-1105. Translation of 1790 ed., Imprenta Universitaria, México.
Holstein N. 2015. Monograph of Coccinia (Cucurbitaceae). PhytoKeys 54: 1–166.
Huang S, Li R, Zhang Z, Li L, Gu X, Fan W, Lucas WJ, Wang X, Xie B, Ni P et al. 2009. The genome of the cucumber, Cucumis sativus L. Nature Genetics 41: 1275–1281.
Jeffrey C. 1980. A review of the Cucurbitaceae. Botanical Journal of the Linnean Society 81: 233–247.
Jiang L, Yan S, Yang W, Li Y, Xia M, Chen Z, Wang Q, Yan L, Song X, Liu R et al. 2015. Transcriptomic analysis reveals the roles of microtubule-related genes and transcription factors in fruit length regulation in cucumber (Cucumis sativus L.). Scientific Reports 5: 8031.
Karlova R, Chapman N, David K, Angenent GC, Seymour GB, de Maagd RA. 2014. Transcriptional control of fleshy fruit development and ripening. Journal of Experimental Botany 65: 4527–4541.
Kates HR, Soltis PS, Soltis DE. 2017. Evolutionary and domestication history of Cucurbita (pumpkin and squash) species inferred from 44 nuclear loci. Molecular Phylogenetics and Evolution 111: 98–109.
Kirkbride JH. 1993. Biosystematic monograph of the genus Cucumis (Cucurbitaceae): botanical identification of cucumbers and melons. Blowing Rock, NC, USA: Parkway Publishers Inc.
Kistler L, Montenegro Á, Smith BD, Gifford JA, Green RE, Newsom LA, Shapiro B. 2014. Transoceanic drift and the domestication of African bottle gourds in the Americas. Proceedings of the National Academy of Sciences, USA 111: 2937–2941.
Kistler L, Newsom LA, Ryan TM, Clarke AC, Smith BD, Perry GH. 2015. Gourds and squashes (Cucurbita spp.) adapted to megafaunal extinction and ecological anachronism through domestication. Proceedings of the National Academy of Sciences, USA 112: 15107–15112.
Kocyan A, Zhang L-B, Schaefer H, Renner SS. 2007. A multi-locus chloroplast phylogeny for the Cucurbitaceae and its implications for character evolution and classification. Molecular Phylogenetics and Evolution 44: 553–577.
Laghetti G, Hammer K. 2007. The Corsican citron melon (Citrullus lanatus (Thunb.) Matsum. et Nakai subsp. lanatus var. citroides (Bailey) Mansf. ex Greb.) a traditional and neglected crop. Genetic Resources and Crop Evolution 54: 913–916.
Larson G, Piperno DR, Allaby RG, Purugganan MD, Andersson L, Arroyo-Kalin M, Barton L, Vigueira CC, Denham T, Dobney K et al. 2014. Current perspectives and the future of domestication studies. Proceedings of the National Academy of Sciences, USA 11: 6139–6146.
Lenser T, Theißen G. 2013. Molecular mechanisms involved in convergent crop domestication. Trends in Plant Science 18: 704–714.
Lust TA, Paris HS. 2016. Italian horticultural and culinary records of summer squash (Cucurbita pepo, Cucurbitaceae) and emergence of the zucchini in 19th-century Milan. Annals of Botany 118: 53–69.
Marr KL, Xia Y-M, Bhattarai NK. 2004. Allozyme, morphological and nutritional analysis bearing on the domestication of Momordica charantia L. (Cucurbitaceae). Economic Botany 58: 435–455.
Marr KL, Xia Y-M, Bhattarai NK. 2005. Allozymic, morphological, phenological, linguistic, plant use and nutritional data on wild and cultivated collections of Luffa aegyptiaca Mill. (Cucurbitaceae) from Nepal, Southern China, and Northern Laos. Economic Botany 59: 137–153.
Marr KL, Xia Y-M, Bhattarai NK. 2007. Allozymic, morphological, phenological, linguistic, plant use, and nutritional data of Benincasa hispida (Cucurbitaceae). Economic Botany 61: 44–59.
Matthews PJ. 2003. Identification of Benincasa hispida (wax gourd) from the Kana archaeological site, Western Highlands province, Papua New Guinea. Archaeology in Oceania 38: 186–191.
Maynard D, Maynard DN. 2000. Cucumbers, melons, and watermelons. In: KF Kiple, KC Ornelas, eds. The Cambridge world history of food. Cambridge, UK: Cambridge University Press, 298–313.
McCreight JD, Staub JE, Wehner TC, Dhillon NPS. 2013. Gone global: familiar and exotic cucurbits have Asian origins. HortScience 48: 1078–1089.
Meyer R, DuVal AE, Jensen HR. 2012. Patterns and processes in crop domestication: an historical review and quantitative analysis of 203 global food crops. New Phytologist 196: 29–48.
Montero-Pau J, Blanca J, Bombarely A, Ziarsolo P, Esteras C, Martí-Gómez C, Ferriol M, Gómez P, Jamilena M, Mueller L et al. 2018. De novo assembly of the zucchini genome reveals a whole-genome duplication associated with the origin of the Cucurbita genus. Plant Biotechnology Journal 16: 1161–1171.
Mote FW. 1977. Yuan and Ming. In: KC Chang, ed. Food in Chinese culture: anthropological and historical perspectives. New Haven, CT, USA: Yale University Press, 193–258.
Murthy KSR, Ravindranath D, Sandhya Rani S, Pullaiah T. 2013. Ethnobotany and distribution of wild and cultivated genetic resources of Cucurbitaceae in the Eastern Ghats of Peninsular India. Topclass Journal of Herbal Medicine 2: 149–158.
Nee M. 1990. The domestication of Cucurbita (Cucurbitaceae). Economic Botany 44: 56–68.
Newstrom LE. 1991. Evidence for the origin of chayote, Sechium edule (Cucurbitaceae). Economic Botany 45: 410–428.
Paris HS. 2015. Origin and emergence of the sweet dessert watermelon, Citrullus lanatus. Annals of Botany 116: 133–148.
Paris HS, Amar Z, Lev E. 2012a. Medieval emergence of sweet melons, Cucumis melo (Cucurbitaceae). Annals of Botany 110: 23–33.
Paris HS, Amar Z, Lev E. 2012b. Medieval history of the duda'im melon (Cucumis melo, Cucurbitaceae). Economic Botany 66: 276–284.
Paris HS, Daunay MC, Janick J. 2013. Medieval iconography of watermelons in Mediterranean Europe. Annals of Botany 112: 867–879.
Paris HS, Lebeda A, Křistkova E, Andres TC, Nee MH. 2012c. Parallel evolution under domestication and phenotypic differentiation of the cultivated subspecies of Cucurbita pepo (Cucurbitaceae). Economic Botany 66: 71–90.
Pickersgill B. 2007. Domestication of plants in the Americas: insights from Mendelian and molecular genetics. Annals of Botany 100: 925–940.
Piperno DR. 2000. Phytoliths in Cucurbita and other Neotropical Cucurbitaceae and their occurrence in early archaeological sites from the lowland American tropics. Journal of Archaeological Science 27: 193–208.
Piperno DR. 2011. The origins of plant cultivation and domestication in the New World tropics: patterns, process, and new developments. Current Anthropology 52: S453–S470.
Piperno DR, Dillehay TD. 2008. Starch grains on human teeth reveal early broad crop diet in northern Peru. Proceedings of the National Academy of Sciences, USA 105: 19622–19627.
Piperno DR, Stothert KE. 2003. Phytolith evidence for early Holocene Cucurbita domestication in southwest Ecuador. Science 299: 1054–1057.
Pyramarn K. 1989. New evidence on plant exploitation and environment during the Hoabinhian (Later Stone Age) from Ban Kao Caves, Thailand. In: DR Harris, GC Hillman, eds. Foraging and farming: the evolution of plant exploitation. London, UK: Unwin Hyman, 282–291.
Qi J, Liu X, Shen D, Miao H, Xie B, Li X, Zeng P, Wang S, Shang Y, Gu X et al. 2013. A genomic variation map provides insights into the genetic basis of cucumber domestication and diversity. Nature Genetics 45: 1510–1515.
Ren Y, Guo S, Zhang J, He H, Sun H, Tian S, Gong G, Zhang H, Levi A, Tadmor Y et al. 2018. A tonoplast sugar transporter underlies a sugar accumulation QTL in watermelon. Plant Physiology 176: 836–850.
Renner SS. 2017. A valid name for the Xishuangbanna gourd, a cucumber with carotene-rich fruits. PhytoKeys 85: 87–94.
Renner SS, Chomicki G, Greuter W. 2014. (2313) Proposal to conserve the name Momordica lanata (Citrullus lanatus) (watermelon, Cucurbitaceae), with a conserved type, against Citrullus battich. Taxon 63: 941–942.
Renner SS, Pandey AK. 2013. The Cucurbitaceae of India: accepted names, synonyms, geographic distribution, and information on images and DNA sequences. PhytoKeys 20: 53–118.
Renner SS, Pérez-Escobar OA, Silber MV, Preick M, Hofreiter M, Chomicki G. 2019. A 3500-year-old genome from a Pharaonic tomb reveals that New Kingdom Egyptians were cultivating domesticated watermelon. bioRxiv doi: 10.1101/642785
Renner SS, Schaefer H. 2016. Phylogeny and evolution of Cucurbitaceae. In: R Grumet, N Katzir, J Garcia-Mas, eds. Genetics and genomics of Cucurbitaceae. Cham, Switzerland: Springer International, 13–23.
Renner SS, Schaefer H, Kocyan A. 2007. Phylogenetics of Cucumis (Cucurbitaceae): cucumber (C. sativus) belongs in an Asian/Australian clade far from melon (C. melo). BMC Evolutionary Biology 7: 58.
Renner SS, Sousa A, Chomicki G. 2017. Chromosome numbers, Egyptian colocynths, and classification of the watermelon genus Citrullus, with 60 names allocated to seven biological species. Taxon 66: 1393–1405.
Rheede HA. 1688. Hortus Malabaricus, vol. 8. V.S. Joannis and D.V. Joannis (repr. ed. 2003). Amsterdam, the Netherlands: Joannis van Dyck, 17–36.
Richter D, Grün R, Joannes-Boyau R, Steele TE, Amani F, Rué M, Fernandes P, Raynal JP, Geraads D, Ben-Ncer A et al. 2017. The age of the hominin fossils from Jebel Irhoud, Morocco, and the origins of the Middle Stone Age. Nature 546: 293–296.
Robinson RW, Decker-Walters DS. 1997. Cucurbits. Wallingford, UK: CAB International, 65–97, 152–163.
Rubatsky VE. 2001. Origin, distribution, and uses. In: DN Maynard, ed. Watermelons: characteristics, production, and marketing. Alexandria, VA, USA: ASHS Press, 21–26.
Ruggieri V, Alexiou KG, Morata J, Argyris J, Pujol M, Yano R, Nonaka S, Ezura H, Latrasse D, Boualem A et al. 2018. An improved assembly and annotation of the melon (Cucumis melo L.) reference genome. Scientific Reports 8: 8088.
Sain RS, Joshi P, Divakara Sastry EV. 2002. Cytogenetic analysis of interspecific hybrids in genus Citrullus (Cucurbitaceae). Euphytica 128: 205–210.
Sanjur OI, Piperno DR, Andres CT, Wessel-Beaver L. 2002. Phylogenetic relationships among domesticated and wild species of Cucurbita (Cucurbitaceae) inferred from a mitochondrial gene: implications for crop plant evolution and areas of origin. Proceedings of the National Academy of Sciences, USA 99: 10923–10928.
Sauer JD. 1993. Historical geography of crop plants: a select roster. Boca Raton, FL, USA: CRC Press.
Schaefer H, Heibl C, Renner SS. 2009. Gourds afloat: a dated phylogeny reveals an Asian origin of the gourd family (Cucurbitaceae) and numerous oversea dispersal events. Proceedings of the Royal Society of London. Series B: Biological Sciences 276: 843–851.
Schaefer H, Renner SS. 2010a. A gift from the New World? The West African crop Cucumeropsis mannii and the American Posadaea sphaerocarpa (Cucurbitaceae) are the same species. Systematic Botany 35: 534–540.
Schaefer H, Renner SS. 2010b. A three-genome phylogeny of Momordica (Cucurbitaceae) suggests seven returns from dioecy to monoecy and recent long-distance dispersal to Asia. Molecular Phylogenetics and Evolution 54: 553–560.
Schaefer H, Renner SS. 2011a. Phylogenetic relationships in the order Cucurbitales and a new classification of the gourd family (Cucurbitaceae). Taxon 60: 122–138.
Schaefer H, Renner SS. 2011b. Cucurbitaceae. In: K Kubitzki, ed. Families and genera of flowering plants, vol. 10. Berlin, Germany: Springer Verlag, 112–174.
Schweinfurth G. 1883. The flora of ancient Egypt. Nature 28: 109–114.
Schweinfurth G. 1884. Über Pflanzenreste aus altägyptischen Gräbern. Berichte der Deutschen Botanischen Gesellschaft 2: 351–371.
Sebastian P, Schaefer H, Lira R, Telford IR, Renner SS. 2012. Radiation following long-distance dispersal: the contributions of time, opportunity and diaspore morphology in Sicyos (Cucurbitaceae). Journal of Biogeography 39: 1427–1438.
Sebastian P, Schaefer H, Telford IR, Renner SS. 2010. Cucumber (Cucumis sativus) and melon (C. melo) have numerous wild relatives in Asia and Australia, and the sister species of melon is from Australia. Proceedings of the National Academy of Sciences, USA 107: 14269–14273.
Shaik RS, Burrows GE, Urwin NA, Gopurenko D, Lepschi BJ, Weston LA. 2017. The biology, phenology and management of Australian weed-camel melon (Citrullus lanatus (Thunb.) Matsum. and Nakai). Crop Protection 98: 222–235.
Shang Y, Ma Y, Zhou Y, Zhang H, Duan L, Chen H, Zeng J, Zhou Q, Wang S, Gu W et al. 2014. Biosynthesis, regulation, and domestication of bitterness in cucumber. Science 346: 1084–1088.
Singh AK. 1978. Cytogenetics of semi-arid plants, III. A natural interspecific hybrid of Cucurbitaceae (Citrullus colocynthis Schrad., C. vulgaris Schrad.). Cytologia 43: 569–574.
Smith BD. 1997. The initial domestication of Cucurbita pepo in the Americas 10,000 years ago. Science 276: 932–934.
Stetter MG, Gates DJ, Mei W, Ross-Ibarra J. 2017. How to make a domesticate. Current Biology 27: R853–R909.
Sun H, Wu S, Zhang G, Jiao C, Guo S, Ren Y, Zhang J, Zhang H, Gong G, Jia Z et al. 2017. Karyotype stability and unbiased fractionation in the paleo-allotetraploid Cucurbita genomes. Molecular Plant 10: 1293–1306.
Telford IRH, Schaefer H, Greuter G, Renner SS. 2011b. A new Australian species of Luffa (Cucurbitaceae) and typification of two Australian Cucumis names, all based on specimens collected by Ferdinand Mueller in 1856. PhytoKeys 5: 21–29.
Telford IRH, Sebastian PM, Bruhl JJ, Renner SS. 2011a. Cucumis (Cucurbitaceae) in Australia and eastern Malesia, including newly recognized species and the sister species to C. melo. Systematic Botany 36: 376–389.
Teppner H. 2004. Notes on Lagenaria and Cucurbita (Cucurbitaceae) - Review and new contributions. Phyton; Annales Rei Botanicae 44: 245–308.
Ter-Avanesyn DV. 1966. Arbuz Kordofanskyi Citrullus lanatus Mansf. ssp. cordophanus Ter-Avan. Botanicheskii Zhurnal 51: 423–426.
Vishnu-Mittre A. 1974. Paleobotanical evidence in India. In J Hutchinson, ed. Evolutionary studies in world crops. Cambridge, UK: Cambridge University Press, 3–30.
Volz SM, Renner SS. 2008. Hybridization, polyploidy, and evolutionary transitions between monoecy and dioecy in Bryonia (Cucurbitaceae). American Journal of Botany 95: 1297–1306.
Volz SM, Renner SS. 2009. Phylogeography of the ancient Eurasian medicinal plant genus Bryonia (Cucurbitaceae) inferred from nuclear and chloroplast sequences. Taxon 58: 550–560.
Walters TW. 1989. Historical overview on domesticated plants in China with special emphasis on the Cucurbitaceae. Economic Botany 43: 297–313.
Wang L, Cao C, Zheng S, Zhang H, Liu P, Ge Q, Li J, Ren Z. 2017. Transcriptomic analysis of short-fruit 1 (sf1) reveals new insights into the variation of fruit-related traits in Cucumis sativus. Scientific Reports 7: 2950.
Wang Y, Xu P, Wu X, Wu X, Wang B, Huang Y, Hu Y, Lin J, Lu Z, Li G. 2018. GourdBase: a genome-centered multi-omics database for the bottle gourd (Lagenaria siceraria), an economically important cucurbit crop. Scientific Reports 8: 3604.
Wasylikowa K, van der Veen M. 2004. An archaeobotanical contribution to the history of watermelon, Citrullus lanatus (Thunb.) Matsum. & Nakai (syn. C. vulgaris Schrad.). Vegetation History and Archaeobotany 13: 213–217.
Watson W. 1969. Early cereal cultivation in China. In: PJ Ucko, GW Dimblebey, eds. The domestication and exploitation of plants and animals. London, UK: Duckworth, 397–402.
Weng Y, Colle M, Wang Y, Yang L, Rubinstein M, Sherman A, Ophir R, Grumet R. 2015. QTL mapping in multiple populations and development stages reveals dynamic quantitative trait loci for fruit size in cucumbers of different market classes. Theoretical and Applied Genetics 128: 1747–1763.
Wu S, Shamimuzzaman M, Sun H, Salse J, Sui X, Wilder A, Wu Z, Levi A, Xu Y, Ling KS, Fei Z. 2017. The bottle gourd genome provides insights into Cucurbitaceae evolution and facilitates mapping of a Papaya ring-spot virus resistance locus. The Plant Journal 92: 963–975.
Yang SL, Pu H, Liu PY, Walters TW. 1991. Preliminary studies on Cucumis sativus var. xishuangbannanesis [sic]. Cucurbit Genetics Cooperative Report 14: 29–31.
van Zeist W, de Roller GJ. 1993. Plant remains from Maadi, a Predynastic site in Lower Egypt. Vegetation History and Archaeobotany 4: 179–185.
Zhang J, Guo S, Ren Y, Zhang H, Gong G, Zhou M, Wang G, Zong M, He H, Liu F et al. 2017. High-level expression of a novel chromoplast phosphate transporter ClPHT4; 2 is required for flesh color development in watermelon. New Phytologist 213: 1208–1221.
Zhang L-B, Simmons MP, Kocyan A, Renner SS. 2006. Phylogeny of the Cucurbitales based on DNA sequences of nine loci from three genomes: implications for morphological and sexual system evolution. Molecular Phylogenetics and Evolution 39: 305–322.
Zheng Y, Wu S, Bai Y, Sun H, Jiao C, Guo S, Zhao K, Blanca J, Zhang Z, Huang S et al. 2019. Cucurbit Genomics Database (CuGenDB): a central portal for comparative and functional genomics of cucurbit crops. Nucleic Acids Research 47: D1128–D1136.
Zhou Y, Ma Y, Zeng J, Duan L, Xue X, Wang H, Lin T, Liu Z, Zeng K, Zhong Y et al. 2016. Convergence and divergence of bitterness biosynthesis and regulation in Cucurbitaceae. Nature Plants 2: 16183.
Zsögön A, Čermák T, Naves ER, Notini MM, Edel KH, Weinl S, Freschi L, Voytas DF, Kudla J, Peres LEP. 2018. De novo domestication of wild tomato using genome editing. Nature Biotechnology 36: 1211–1218.

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Volume226, Issue5

June 2020

Pages 1240-1255

Origin and domestication of Cucurbitaceae crops: insights from phylogenies, genomics and archaeology

Summary

I. Introduction

II. The diversity of cultivated Cucurbitaceae: traits of major and minor crops

III. Time and place of domestication

1. The New World as a centre of cucurbit domestication

2. Africa as a centre of cucurbit domestication

3. Asia and Melanesia as centres of cucurbit domestication

IV The genomics of Cucurbitaceae domestication

1. Loss of bitterness

2. Selection for sweetness

3. Selection for larger fruits

4. Seed traits

5. Selection for high carotenoid content

V. Conclusions

Acknowledgements

References

Citing Literature

Figures

References

Information

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Origin and domestication of Cucurbitaceae crops: insights from phylogenies, genomics and archaeology

Summary

I. Introduction

II. The diversity of cultivated Cucurbitaceae: traits of major and minor crops

III. Time and place of domestication

1. The New World as a centre of cucurbit domestication

2. Africa as a centre of cucurbit domestication

3. Asia and Melanesia as centres of cucurbit domestication

IV The genomics of Cucurbitaceae domestication

1. Loss of bitterness

2. Selection for sweetness

3. Selection for larger fruits

4. Seed traits

5. Selection for high carotenoid content

V. Conclusions

Acknowledgements

References

Citing Literature

Figures

References

Related

Information