This online reprint from the American Journal of Botany describes the domestication, cultivation and dispersal of prickly pear cactus (Opuntia), from its Central Mexican and pre-Aztec origins to present-day naturalization throughout the Mediterranean region and elsewhere in the arid and semi-arid world.

Abstract

Opuntia ficus-indica is a long-domesticated cactus crop that is important in agricultural economies throughout arid and semiarid parts of the world. The biogeographic and evolutionary origins of this species have been obscured through ancient and widespread cultivation and naturalization. The origin of O. ficus-indica is investigated through the use of Bayesian phylogenetic analyses of nrITS DNA sequences. These analyses support the following hypotheses: that O. ficus-indica is a close relative of a group of arborescent, fleshy-fruited prickly pears from central and southern Mexico; that the center of domestication for this species is in central Mexico; and that the taxonomic concept of O. ficus-indica may include clones derived from multiple lineages and therefore be polyphyletic.

Key Words: archaethnobotany • Bayesian analysis • crop origins • Opuntia • Opuntia ficus-indica

Introduction

Opuntia ficus-indica (L.) Mill. is a crop species (Fig. 1) that figures prominently in the modern folklore of ethnobotany. The narrative of Luther Burbank's development and promotion of certain clones of O. ficus-indica in the early 20th century is vividly chronicled (with sharp wit) by Benson (1982). Opuntioid cacti are recognized as ideal crops for arid regimes (Felger 1979, Russell and Felker 1987) because Opuntia ficus-indica is extremely efficient at converting water into biomass (Kluge and Ting 1978). Opuntia ficus-indica, one of several long-domesticated cactus species (Casas et al. 1997, Casas and Barbera 2002), is the most widespread and economically important of these cactus crops (Nobel 2002, Nobel et al. 2002), as important as corn and tequila agave in the agricultural economy of modern Mexico (Barrientos 1966). The facile introgression of Opuntia is very well documented; this genus is among the most interspecifically promiscuous plants, perhaps rivaled only by Quercus L. in this regard (Benson and Walkington 1965; Grant and Grant 1971b, 1979; Felger 1979; Baker and Pinkava 1987, 1999; Griffith 2001a, b, 2003; Pinkava 2002; among others). The relative ease of vegetative propagation of Opuntia is demonstrated by its occasional clonal dominance of certain areas (Grant and Grant 1971a, Mandujano et al. 1996). This aspect of Opuntia marks it as a noxious weed in some places (Dodd 1936, Nobel 1994). This ease of clonal propagation was probably not lost on the very early human population of the New World. Evidence exists for the use of Opuntia as human food at least 9000 years before the present (Kiesling 1998) or even as early as 12 000 years ago (Callen 1967), probably before cultivation (Ostolaza 1994).

Opuntia ficus-indica is used in numerous ways. In modern times, first and foremost, O. ficus-indica is grown for the large, sweet fruits (often called "tunas"), which are available in local and commercial markets worldwide (Basile 2001, Inglese et al. 2002). Important tuna-growing regions include Mexico, Sicily, Algeria, Chile, Brazil, and northern Africa (Barbera et al. 1992, Inglese et al. 2002). In addition, the young cladodes (stem segments) of O. ficus-indica are harvested as a vegetable crop (often called nopalitos). Although this crop is less valuable worldwide than the fruit crop, vegetable products of O. ficus-indica are available in many local and commercial markets (Sáenz-Hernandez et al. 2002). Various other uses have been reported for O. ficus-indica, including as a binding and waterproofing agent in adobe (Cárdenas et al. 1998). Medicinal properties of O. ficus-indica have been documented as early as 1552 (Emmart 1940). Opuntia ficus-indica (along with other Opuntia and Nopalea species) has been grown from pre-Columbian times as a host plant for cochineal insects (Dactylopius coccus) for the production of valuable, vivid red and purple dyes (Donkin 1977, Nobel 1994). See Anderson (2001) for a near-exhaustive review of the various other uses of O. ficus-indica.

Early European botanists (often referring to Pliny or Theophrastus) called this cactus Ficus indica (Donkin 1977), although some found this to be an unsuitable name, as the plant did not resemble the Indian fig (possibly Ficus benghalensis L.) already known (Anderson 2001). Linnaeus published Cactus opuntia and C. ficus-indica in Species Plantarum. Miller combined these into Opuntia ficus-indica in 1768. In the recorded history of the Old World, O. ficus-indica was certainly known at the beginning of the 16th century (Donkin 1977, Casas and Barbera 2002), and it is believed that this species accompanied Columbus in his first return to Lisbon in 1493 (Russell and Felker 1987, Anderson 2001), placing O. ficus-indica in the Caribbean by at least the late 1400s, although whether it is native there is unknown. The plants are also recorded in cultivation in Tlaxcala, Mexico, in 1519 (Diaz del Castillo 1632 in Idell 1957). Opuntia ficus-indica fruits and shoots were also reportedly consumed by the Maya of southeastern Mexico (Coe 1994). There is also some evidence for the use of O. ficus-indica by the Nazca of Peru, placing these plants in South America at a very early date (Sejuro 1990). Other workers maintain that this taxon was unknown in pre-Columbian South America (Towle 1961, Baker 2002). The succulent, ever-fresh cladodes were certainly a novelty to late 15th century and later Europeans (Donkin 1977) and were widely included in ships' stores as insurance against scurvy (Kiesling 1998). This practice is thought to have contributed greatly to the present naturalized range of Opuntia ficus-indica throughout arid and semiarid habitats of the world (Anderson 2001, Casas and Barbera 2002, Sáenz-Hernandez et al. 2002). This widespread propagation (intended and unintended) throughout the Mediterranean obscured the geographic origins of this species; many early European botanists regarded this cactus to be native (Donkin 1977, Barbera et al. 1992), as reflected in Cactus opuntia L. (i.e., spiny plant from near Opus, Greece; Anderson 2001). This Mediterranean naturalization may now be conceived as complete, as the Israelis of the mid-20th century often adopted the (believed-indigenous) sabras as a symbol of their struggle (and humanity) in adverse desert conditions (Uris 1959).

Although most recent authors concede that this species is not native to the Old World, the geographic and evolutionary origins of Opuntia ficus-indica remain clouded in obscurity (Britton and Rose 1919, Bravo-Hollis 1978, Benson 1982, Anderson 2001). This mystery arises partly from the widespread cultivated distribution of the plants, both within and away from the New World (Anderson 2001), but also from the phenotypic variability and artificial selection of the plants (Benson 1982). The specific epithet (from P. Miller, 1768) may reflect the 16th-century European opinion that the plants are native to the West Indies (Barbera et al. 1992, Casas and Barbera 2002). The name "tuna" is Caribbean in origin (Bravo-Hollis 1978, Kiesling 1998). Other early work proposed that O. ficus-indica was a spineless cultivar derived from O. megacantha, a species of central Mexico (Griffiths 1914). A recent, important paper explored this relationship with amplified fragment length polymorphism (AFLP) data and reported that O. ficus-indica had the closest affinity with O. megacantha (Labra et al. 2003), corroborating the Griffiths (1914) hypothesis. Other authors, however, consider O. megacantha also to be a cultivated taxon (Benson, 1982) or a name applied to multiple ruderal reversions to spininess from escaped, cultivated O. ficus-indica (Kiesling 1998) and treat O. megacantha as a later synonym (Benson 1982, Kiesling 1998). Uphof (1968) and Zeven and Zhukovsky (1975, page 164) place the origin of this cactus within "Mexico" or the "Central American and Mexican centre" of domestication, but without reference to a specific region. Some recent cytological work proposes that octoploid, cultivated O. ficus-indica is derived from a diploid Mexican (but unnamed) progenitor (Kiesling 1998). Benson (1982) states that O. ficus-indica is native to mild tropical upland habitat (not deserts), but does not state where. Given the conflicting, sometimes confusing, and often unclear hypotheses as to the origins of this cactus crop, a wide molecular phylogenetic analysis has potential to elucidate the biogeography of this species. The current study addresses the biogeographic and evolutionary origins of O. ficus-indica through modern molecular means. To this end, I have gathered and analyzed DNA sequence data from a number of accessions of O. ficus-indica representing plantings throughout the world.