Evening primrose [Greek oinos, wine, and thera, seeking or catching, alluding to roots of some unknown plants possessing perfume of wine, perhaps misapplied by Linnaeus]

Warren L. Wagner

Herbs, annual, biennial, or perennial, sometimes suffrutescent, caulescent or acaulescent; usually with taproots, sometimes fibrous roots, sometimes with shoots arising from spreading lateral roots, or with rhizomes. Stems erect or ascending, sometimes decumbent, and then sometimes rooting at nodes, epidermis green or whitish and exfoliating. Leaves in basal rosette and cauline, basal leaves present before flowering, often absent later, alternate; stipules absent; sessile or petiolate; blade margins toothed to pinnatifid, often irregularly so, sometimes subentire. Inflorescences: flowers solitary in leaf axils, when terminal, often forming leafy spikes, rarely racemes, erect or nodding. Flowers bisexual, usually actinomorphic, sometimes zygomorphic and petals positioned in upper 1/2 of flower (in sect. Gaura), buds erect or recurved; floral tube deciduous (with sepals, petals, and stamens) after anthesis, usually glabrous, sometimes lanate or densely hispid, with short, interlocking hairs within, with basal nectary; sepals (3 or)4, reflexed individually, in pairs, or as a unit and reflexed to one side at anthesis; petals (3 or)4, usually yellow, purple, or white, rarely pink or red, sometimes base pale green to yellow, usually fading orange, purple, pale yellow, reddish, or whitish; stamens (6 or)8, subequal or in 2 unequal series, anthers versatile, filaments usually without basal scale, sometimes with basal scale (sect. Gaura), 0.3–0.5 mm, scales nearly closing mouth of floral tube, pollen shed singly; ovary (3 or)4-locular or septa incomplete (sect. Gaura) and 1-locular, ovules numerous, or 1–8 (sect. Gaura), style glabrous or pubescent, stigma usually deeply divided into (3 or)4 linear lobes, sometimes peltate, discoid to nearly quadrangular or obscurely and shallowly 4-lobed (sect. Calylophus), entire surface of lobes receptive, surface probably wet and non-papillate, subtended by ± conspicuous peltate indusium in early development, persisting to anthesis, often obscured by developing stigma. Fruit a capsule, straight or curved, lanceoloid or ovoid, ellipsoid to cylindrical, rhombic-obovoid, or globose, sometimes clavate or ellipsoid with proximal part sterile and cylindrical, tapering to a pedicel-like base (stipe), terete or (3 or)4-angled or -winged, usually loculicidally dehiscent, sometimes tardily so, sometimes an indehiscent, nutlike capsule with hard, woody walls (sects. Gaura, Gauropsis), usually (3 or)4-locular, sometimes septa incomplete and fragile and then ovary 1-locular (sect. Gaura); usually sessile, sometimes pedicellate. Seeds usually numerous (1–160+), in 1 or 2(–4) rows or clustered in each locule, or sometimes reduced to 1–8 (sect. Gaura), surface papillose, beaded, rugose, furrowed, reticulate, or smooth. x = 7.

Species ca. 150 (93 in the flora): North America, Mexico, West Indies, Bermuda, Central America, South America; introduced in temperate to subtropical areas nearly worldwide.

Oenothera is distributed widely in temperate to subtropical areas of North America and South America, usually in open, often disturbed habitats, from sea level to nearly 5000 m elevation; several species are widely naturalized worldwide. The center of diversity for Oenothera is in southwestern North America, but farther east than other genera of the Onagreae. Oenothera is delimited here more broadly than in the past, when as many as 15 genera were recognized, which broadly correspond to sections recognized here, and as few as three (P. A. Munz 1965) or four genera (P. H. Raven 1964). Oenothera, as it has been delimited in recent decades, lacked a clear generic synapomorphy, but was considered distinctive by virtue of having a 4-lobed stigma receptive over its entire surface; however, Gaura, Stenosiphon (short lobes with a distinctive disk at the base), and to some degree Calylophus (peltate, discoid to quadrangular, sometimes shallowly 4-lobed) each have similar but slightly different variations on the basic lobed stigma. Calylophus and Gaura have been considered to be closely related and distinct from Oenothera and Stenosiphon by having anthers with both tapetal and parenchymatous septa (Raven). Molecular studies with broad sampling in Onagreae (R. A. Levin et al. 2004) showed high support for a monophyletic Oenothera only when Calylophus, Gaura, and Stenosiphon are included within it. Subsequently, it was recognized that while stigma morphology varies among these four groups from deeply divided into long or short linear lobes to peltate, discoid, nearly square or obscurely and shallowly 4-lobed, the stigmas of all four groups are subtended by a more or less conspicuous peltate indusium (W. L. Wagner et al. 2007). This structure, long known in Gaura and Stenosiphon because it is conspicuous throughout anthesis, had been overlooked in Oenothera, apparently because it usually is evident only in early development; in some species it becomes less conspicuous and even hidden by the stigma. Molecular analyses (Levin et al.; G. D. Hoggard et al. 2004) and the consistent synapomorphy of the indusiate style lead to a broadened concept of Oenothera (Wagner et al.) by including in it the previously separate genera Gaura and Stenosiphon for the first time. Calylophus is also included in the expanded Oenothera as was done by Munz and others, but not by Raven and H. F. Towner (1977).

Permanent translocation heterozygosity (PTH) appears to have been a major element in the evolution of species of Oenothera (R. E. Cleland 1972; P. H. Raven 1979; K. E. Holsinger and N. C. Ellstrand 1984; C. Harte 1994; W. Dietrich et al. 1997; M. T. Johnson et al. 2009, 2011), and otherwise occurs in the Onagraceae only in Gayophytum heterozygum. Permanent translocation heterozygosity has been recorded in only 57 species in seven plant families (for example, Holsinger and Ellstrand), including Onagraceae (47 spp.), Campanulaceae (2 spp.), Commelinaceae (2 spp.), Clusiaceae (2 spp.), Iridaceae (3 spp.), Paeoniaceae (2 spp.), and Papaveraceae (1 sp.). The taxonomic distribution of PTH in the Onagraceae now appears to be even more concentrated in Oenothera than when Raven reviewed PTH in the family; in his treatment, PTH occurred in Calylophus (1 sp.), Gaura (2 spp.), Gayophytum (1 sp.), and Oenothera (43 spp., including 37 in sect. Oenothera, and the other six in sections now included in one of the two primary Oenothera lineages [including Hartmannia (1 sp.), Kneiffia (1 sp.), Lavauxia (1 sp.), Leucocoryne (2 spp.), and Xanthocoryne (1 sp.)]. It appears that the specific chromosomal structure in Oenothera—metacentric chromosomes with pycnotic, condensed proximal regions—enables reciprocal translocations, resulting in the regular occurrence of rings of chromosomes at meiosis and ultimately the specialized system of PTH, in which all seven pairs of chromosomes exchange arms and segregate as a unit (M. Kurabayashi et al. 1962; Cleland; Raven). The best known species possessing this system are the members of subsect. Oenothera, in which the structure and mechanisms of PTH were elucidated (Cleland; Harte; Dietrich et al.). In addition to the translocations, the system requires balanced lethals, which prevent the formation of the homozygous combinations (PTH species have ca. 50% infertile pollen (sterile pollen smaller than fertile under minimal magnification, but fertility can range from 30% to 85%), facultative autogamy, and alternate disjunction of the chromosomes during meiosis. In PTH species, a ring of 14 chromosomes or occasionally 12 + 1 pair chromosomes is formed at meiotic metaphase. A PTH species in the sense employed here is an aggregation of true-breeding populations having similar morphological and genetic attributes.

P. H. Raven (1979) pointed out that most PTH species are annuals or biennials; only about 10% of the known PTH species in Onagraceae are perennial. Most of the species of Oenothera that have become naturalized outside their natural range are PTH, and all of the species that have achieved a wide naturalized distribution are PTH. Most of the PTH species in Oenothera seem to have originated within the limits of a taxonomic species (Raven). In a few instances, notably O. triangulata (Raven and D. P. Gregory 1972[1973]), four species of subsect. Oenothera (Raven et al. 1979; W. Dietrich et al. 1997), and several species of subsect. Munzia (Dietrich), the PTH taxa seem to have originated after hybridization between species. In all instances, PTH seems to have arisen as a way to limit recombination (Raven). In Oenothera, floating translocations are common (that is, a ring of four or a ring of six) and 46 species (30% of the species in the genus) are PTH with 1II + a ring of 12 chromosomes or a ring of 14.

Evening primrose oil (EPO), found mainly in seeds of sect. Oenothera, contains a rare omega-6 essential fatty acid, gamma-linolenic acid (GLA), which is considered to be the active therapeutic ingredient with value as a pharmaceutical and nutritional supplement. EPO is used for the treatment of a variety of disorders, particularly those affected by metabolic products of essential fatty acids; convincing evidence for its efficacy in treating most disorders is still lacking. The most promising uses are in the treatment of eczema and other skin irritations, multiple sclerosis, and diabetes.

Many species of Oenothera are cultivated and are among the most popular ornamentals in the family. The species most commonly cultivated and used for creating horticultural cultivars are O. Capillifolia (sect. Calylophus), O. Lindheimeri (sect. Gaura), O. Speciosa (sect. Hartmannia), O. Fruticosa (sect. Kneiffia), O. Acaulis and O. Flava (sect. Lavauxia), O. Macrocarpa (sect. Megapterium), O. Glazioviana (sect. Oenothera), and O. Cespitosa (sect. Pachylophus).

Reproductive features include: self-incompatible or self-compatible; flowers vespertine or diurnal, usually lasting less than one day, but sometimes lasting two to several days (sects. Kneiffia, Megapterium); outcrossing species with diurnal flowers pollinated by bees [especially Halictidae (halictids), Anthophoridae (anthophorids), and Bombus], small moths, butterflies, syrphid flies, or hummingbirds (two spp.), and outcrossing species with vespertine flowers pollinated by hawkmoths or, sometimes, other small moths, rarely wasps or antlions (in O. Cinerea of sect. Gaura), or autogamous, occasionally cleistogamous.

Seed numbers are not known precisely for all sections of Oenothera; here, seeds numerous indicates usually 30+ per capsule; for some taxa, seed number ranges from one to eight per capsule; when eight or fewer, the actual range is usually given.

Several sections (for example, Gaura, Hartmannia, Kneiffia, Leucocoryne, Peniophyllum) of Oenothera have capsules much wider in the distal, fertile part than in the proximal, sterile part, which tapers to a pedicel-like stipe. In other sections (for example, Megapterium, Pachylophus) the proximal part of the capsule is abruptly constricted to what has traditionally been considered to represent a pedicel. That terminology has been continued here, but anatomically it is not clear whether the stalk in these sections is developmentally the same as those with a stipe. The origin of pedicel-like structures should be studied in depth across the family.

SELECTED REFERENCES Cleland, R. E. 1972. Oenothera: Cytogenetics and Evolution. London. Evans, M. E. K. et al. 2005. Climate and life-history evolution in evening primroses (Oenothera, Onagraceae): A phylogenetic comparative analysis. Evolution 59: 1914–1927. Evans M. E. K. et al. 2009. Climate, niche evolution, and diversification of the “bird-cage” evening primroses (Oenothera, sections Anogra and Kleinia). Amer. Naturalist 173: 225–240. Gregory, D. P. 1963. Hawkmoth pollination in the genus Oenothera. Aliso 5: 375–384. Gregory, D. P. 1964. Hawkmoth pollination in the genus Oenothera. Aliso 5: 385–419. Harte, C. 1994. Oenothera: Contributions of a Plant to Biology. Berlin. Stubbe, W. 1964. The role of the plastome in the evolution of the genus Oenothera. Genetica 35: 28–33. Tobe, H., W. L. Wagner, and Chin H. C. 1987. Systematic and evolutionary studies of Oenothera (Onagraceae): Seed-coat anatomy. Bot. Gaz. 148: 235–257. Wagner, W. L. 2005. Systematics of Oenothera sections Contortae, Eremia, Pachylophus, and Ravenia (Onagraceae). Syst. Bot. 30: 332–355.