Correct names for some of the closest relatives of Carica papaya: A review of the Mexican/Guatemalan genera Jarilla and Horovitzia

Abstract Using molecular data, we recently showed that Carica papaya L. is sister to a Mexican/Guatemalan clade of two genera, Jarilla Rusby with three species and Horovitzia V.M. Badillo with one. These species are herbs or thin-stemmed trees and may be of interest for future genomics-enabled papaya breeding. Here we clarify the correct names of Jarilla heterophylla (Cerv. ex La Llave) Rusby and Jarilla caudata (Brandegee) Standl., which were confused in a recent systematic treatment of Jarilla (McVaugh 2001). We designate epitypes for both, provide weblinks to type specimens, a key to the species of Jarilla and Horovitzia, and notes on their habitats and distribution.


Introduction
Th e family Caricaceae Dumort. comprises 34 species and one formally named hybrid in currently six genera. A molecular phylogeny that included all species revealed that Carica papaya L. (the only species in the genus Carica ) is sister to a clade of four species endemic to Mexico and Guatemala (Carvalho and Renner 2012). Th e discovery that the closest relatives of C. papaya are three herbs in the genus Jarilla Rusby and a thin stemmed tree, Horovitzia cnidoscoloides (Lorence & R. Torres) V. M. Badillo, has implications for plant breeders, who have so far tried in vain to cross papaya with tree species in the genus Vasconcellea A. St.-Hil., known as the highlands papayas. To facilitate communication among researchers from diff erent fi elds, and since full-genome sequencing of the species of Jarilla and Horovitzia is ongoing (R. Ming, Urbana-Champaign, personal communication, Aug. 2013), we here provide a conspectus of the four species that are the closest relatives of papaya and clean up a nomenclatural confusion involving two names in the genus Jarilla .
We start with the nomenclatural issues, then provide a key to the four species, and end with brief comments on the range and habitat of each species.

Nomenclature of Jarilla
Pablo de La Llave (1832), a director of the National Museum of Natural History of Mexico, was the fi rst to describe one of the unusual herbaceous Caricaceae that are today placed in Jarilla . He had access to fruiting specimens only and based his description of the fl owers on notes made by Vicent Cervantes, a professor of botany in Mexico City and one of the founders of that city's botanical garden in 1788. La Lave gave his new species the epithet "heterophilla" [sic] to refer to its variably shaped leaves. To mark the distinctness of the new species, he placed it in a separate genus, Mocinna , honoring the Mexican naturalist José Mariano Mociño. Unfortunately, this overlooked that Lagasca in 1816 had already described an Asteraceae genus by that name. Soon thereafter, George Bentham (1839) described the same species as Carica nana , based on an unnumbered Hartweg specimen ( Fig. 1) collected in 1836 in Léon (Guanajuato, Mexico). Th e holotype at K (Fig. 1) bears the number 288 on its label, a number corresponding to the page of Plantae Hartwegianae on which C. nana was described. Diaz-Luna and Lomeli-Sención (1992), in their revision of Jarilla , cite this collection as Hartweg 255 (K), probably due to a misreading of 288 for 255.
Th e second herbaceous Caricaceae species was named in March 1894 by Townshend S. Brandegee, who described Carica caudata from the Cape region of Baja California, Mexico, based on a plant he collected the year before (Fig. 2). In August of the same year, José Ramírez, unaware of Brandegee's publication, described a new variety of the fi rst herbaceous Caricaceae, M. heterophylla La Llave, naming it varietas sesseana , based on living plants from Guanajuato and Jalisco. Unfortunately, he appears to have made no herbarium specimens, but only two beautiful plates showing the typical variety and var. sesseana (Fig. 3). Comparison of the plate of var. sesseana and the holotype of C. caudata leaves no doubt that these names refer to the same species, and we therefore agree with previous assessments (Diaz-Luna andLomeli-Sención 1992, Badillo 1993) that they are synonyms.
Realizing that Mocinna La Llave was a younger homonym of Mocinna Lag., Henry Hurd Rusby (1921) proposed the substitute name Jarilla , derived from the Spanish vernacular name Jarrila, for M. heterophylla . He also up-ranked var. sesseana as a separate species, Jarilla sesseana (Ramírez) Rusby . We agree with Diaz-Luna and Lomeli-Sención (1992) and McVaugh (2001) that Rusby's publication of the substitute name Jarilla meets the requirement for valid publication and that Ivan M. Johnston's (1924) slightly later publication of the name Jarrilla (the correct Spanish spelling) to replace Mocinna is a superfl uous name. At around the same time, Standley (1924) realized that Carica caudata Brandegee belonged in Jarilla and was in fact an older name for J. heterophylla var. sesseana Ramírez (= Jarilla sesseana (Ramírez) Rusby), and he accordingly changed the name to J. caudata . He also described a third herbaceous species of Caricaceae, Jarilla chocola Standley, based on two collections made in 1935 from Sonora, Mexico (Standley 1937).
Th us, by 1937 it was clear there were three species of Jarilla and also what their correct names were. In their revision of the genus, Diaz-Luna and Lomeli-Sención (1992) designated plate II of Ramírez (1894;our Fig. 3 left-hand plate) as the lectotype of J. heterophylla var. sesseana and plate V as the neotype of var. heterophylla (our Fig. 3 right-hand plate). Unfortunately, the most recent study of Jarilla , that of Rogers McVaugh (2001), synonymized the two taxa distinguished by Ramírez. Th is error is surprising given the diff erent leaves and fruits of Ramírez's two varieties (our Fig. 3), and indeed McVaugh seems to have been aware he might be making a mistake because he writes (2001: 469), "In the following I have drawn heavily upon the work of Diaz-Luna and Lomelí-Sención, whose personal observations of these interesting species greatly increased our knowledge of them, and have indeed provided almost all the available information about the living plants. Errors introduced here, as a result of faulty translation or interpretation of the work of these authors, or otherwise, are solely my responsibility. " We agree with Diaz-Luna and Lomeli-Sención (1992) and the earlier workers cited above that Jarilla heterophylla var. heterophylla is the oldest name for Bentham's Carica nana , while var. sesseana is a younger synonym of Carica caudata. We have accordingly up-dated the names of our previous Jarilla heterophylla and J. nana sequences in GenBank (Carvalho and Renner 2012; all of which are vouchered). Together, the descriptions of Ramírez (1894), Brandegee (1894), Rusby (1921), Johnson (1924, Standley (1924), and Diaz-Luna and Lomeli-Sención (1992) provide a clear idea of the morphological distinctions of the two species: Jarilla caudata has rounded to ovate or deltoid (never hastate) leaves, c. 1 cm (rarely longer) male fl owers, and 10 cm long fruits that are narrowed at the base with fi ve horn-like appendages, each 3-6 cm long (Fig. 4). Jarilla heterophylla has hastate leaves, 0.5 cm long male fl owers, and c. 3 cm long fruits with short and thick appendages as shown in Fig. 5.
To fi x the usage of the two names more reliably, we below designate epitypes to serve as interpretative specimens for plates II and V of Ramírez (1894), following Art. 9.8 of the Melbourne Code (McNeill et al. 2012). Th e plates published by Ramírez fail to include staminate and pistillate fl owers for both species and therefore do not precisely fi x the application of the names of these dioecious species. In addition, physical specimens also can help in evolutionary studies because they can yield DNA that may be used in future comparisons. We chose as epitypes complete male and female specimens from the same population. Th e epitypes are deposited in M. Isoepitypes of Mocinna heterophylla Cerv. ex La Llave var. sesseana (= Jarilla caudata (Brandegee)   Mature fruits 2-4 cm long with 5 curved basal appendages 0.5-2 cm long. Seeds light brown, 2.5-3.5 mm long. Male fl owers in general <1 cm (  Jarilla chocola is an erect herb, with mostly lobate leaves and fruits with 5 longitudinal wings. Th e species occurs at low altitudes (100-1300 m) along the Pacifi c Coast from Sonora to El Salvador. Remarks. Jarilla caudata is morphologically and phylogenetically closely related to J. heterophylla. Th eir main distinguishing features are the fruits, which in J. caudata can attain a length of 30 cm, having a smooth surface and 5 long, horn-like appendages (3-6 cm long). Other diff erences are given in the key. Th e species occurs in deciduous forests and fi elds of Baja California and central Mexico from 1500 to 1800 m above sea level. Remarks. For diff erences from Jarilla caudata see under that species and in the key. Jarilla heterophylla occurs in oak forests, deciduous forests, and abandoned fi elds of central Mexico at 1500 to 2700 m above sea level.