Resurrection of the genus Aphyllon for New World broomrapes (Orobanche s.l., Orobanchaceae).

Recent phylogenetic studies support a monophyletic clade of New World broomrapes (Orobanche sects. Gymnocaulis and Nothaphyllon) sister to the Old World genus Phelipanche. I place the New World taxa in the genus Aphyllon, propose 21 new combinations, and provide a list of currently accepted taxa.

Introduction

Phylogenetic analysis of broomrapes and related holoparasites using nuclear DNA have found that the small eastern Mediterranean genus Nicolson is nested within sensu lato (s.l.) as circumscribed by Beck (1890) (Schneeweiss et al. 2004a). Morphological and cytological differences between groups of taxa within s.l. have led some botanists to adopt a narrower generic circumscription. In this taxonomic concept, sensu stricto is limited to Old World species that lack bracteoles and have a base chromosome number of x = 19, a calyx divided to the base, and generally unbranched stems (Holub 1977, 1990). Other Old World broomrapes are treated as Pomel or the monotypic genus F.W. Schultz PageBreak(syn: Wallr. and (F.W. Schultz) Batt., respectively; Joel 2009; Schneweiss 2013).

Broomrape species native to the New World constitute two well-supported clades that together form a clade sister to (Schneider et al. 2016). Taxonomically, these clades have been recognized as two separate genera (= Nutt.) and Phil. (= (A. Gray) Heckard) by Holub (1977, 1990) and others (Schneweiss 2013), or more rarely, together as s.l. (Gray 1876). However, neither of these generic taxonomies has been widely adopted among American botanists, in part because of the lack of available names for many taxa. Providing evidence to support the treatment of all New World broomrapes as and a providing list of recognized species (with homotypic synonymns) is the purpose of this paper. New combinations are made where appropriate.

Methods

In order to compare molecular branch lengths of major clades of s.l., a phylogram of and related holoparasites was inferred from 3 nuclear DNA loci (ITS, phytochrome A, and phytochrome B). All sequences were downloaded from Genbank, aligned, and concatenated into a supermatrix using SUMAC (Freyman 2015). The ML phylogeny was estimated using RAxML (Stamatakis 2014) with a GTR+Γ nucleotide substitution model and 1000 rapid bootstrapping replicates.

maximum likelihood

Information about type specimens, basionyms, and synonomy of these new combinations was gathered by examining protologues and images of type specimens using major databases, including Tropicos (http://www.tropicos.org), JSTOR Global Plants (http://plants.jstor.org), and the International Plant Names Index (http://www.ipni.org). Types for all North American taxa and Mattf. have been designated by previous authors and are presented here. For three of the four South American taxa, typification would require more careful efforts beyond the scope of this article. No repository is given in the protologue for two syntypes of Mattf. (Woitschach 71 and F. J. F. Meyen s.n.). The current existence of these specimens could not be verified, although a photograph of the Woitscach 71 (possibly from a specimen at B) is available at F. No specimens are cited by Rodolfo Phillipi in the protologues of the two taxa that he described.

Discussion

Molecular phylogenetic analyses have consistently supported a sister-group relationship between two strongly supported two American clades, representing and (McNeal et al. 2013; Schneider et al. 2016; Fig. 1). This relationship is supported by biogeography and synapomorphies such as a calyx with five fully developed lobes and a base chromosome number of x = 12, with polyploidy in most PageBreaktaxa (Heckard and Chuang 1975; Schneeweiss et al. 2004b). Holub (1977, 1991) has proposed treating the American broomrapes as two genera rather than one, though this was likely due to his erroneous belief based on vegetative morphology that is most closely related to and that is allied to (Holub, 1977).

Figure 1.

Maximum likelihood (ML) phylogram of and related holoparasite species inferred from 3 nuclear DNA loci (ITS, phytochrome A and phytochrome B). Bootstrap support values >70% are labeled. Due to space constraints, several clades have been collapsed. For a more detailed and thorough study of phylogenetic relationships within , see Schneider et al. (2016).

The genus was described by Mitchell (1769), although it was not until nearly 80 years later that Asa Gray made a combination for A. Gray. This species was the only broomrape included in his Manual of the Botany of the Northern United States (1848), though in the second edition (1856) Gray recognized two additional species. Gray limited his generic concept for to taxa assignable to , instead recognizing Nutt. in Tourn. ex Desf. However, after a study of the Californian flora, Gray amended his generic concept of to include two sections, and , together containing all taxa native to the New World (Gray 1876). Though expanded from Gray’s initial circumscription, it was appropriate given Michell’s original diagnosis of as having a five-toothed calyx (“semiquinquefidum”), a synapomorphy of New World broomrapes. A generation later, Rydberg (1906) proposed elevating Gray’s to genus rank on the basis of differences in habit and placentation using the available name Phil. However, the broader generic concept of used by Beck (1890) has prevailed, particularly among American botanists.

Due to the biogeographical, morphological, cytological, and phylogenetic affinities of the New World broomrapes, I recommend treating them in a single genus, , composed of sections (= ) and (= ). Below, I present a key to sections and a list of recognized taxa in PageBreak, proposing new combinations as necessary. Combinations are made at the most recently treated rank for the taxon in , with the exception of subsp. occidentale Greene, which is recognized at species rank under the available name (A. Heller) Holub due to its unique hosts, long molecular branch lengths, and recent discovery of sympatric populations of and in southwestern British Columbia (Schneider et al. 2016). The treatment of should be considered tentative; further taxonomic study is underway which will result in the recognition of several additional taxa.

Taxonomic treatment

Mitch., Diss. Brevis. Princ. Bot. 43. 1769.

Raf. Neogenyton 3. 1825. [Type:

Endl.,

Raf. ex Britton,

Type.

(L.) Torr. & A. Gray, Manual 290. 1848.

Description.

Herb, annual or rarely perennial, achlorophyllous, holoparasitic. Stems fleshy. Leaves reduced to scale-like bracts. Inflorescences terminal racemes, spikes, corymbs, or panicles. Calyx 5-toothed. Corolla sympetalous, bilabiate to regular, tubular and often curved. Style long, stigma crateriform and peltate, or bilamellar. Fruit loculicidal capsules.

About 22 species: 18 in North America, 4 in South America.

Nutt., Gen. N. Amer. Pl. [Nuttall]. 2: 59. 1818.

Stems subterranean or rising to about ground level. Pedicels long and slender, much longer than flower. Bracteoles subtending the calyx absent.

(Nutt.) Torr & A. Gray, Manual (ed. 2) 281. 1848.

Nutt., Gen. N. Amer. Pl. 2: 59. 1818.

(Nutt.) Spreng., Syst. Veg. [Sprengel] 2: 818. 1825.

(Nutt.) Raf., Neogenyt. 3. 1825.

(Nutt.) G. Don., Gen. Hist. 4: 633. 1838.

(Nutt.) Walp., Repert. Bot. Syst. 3: 480. 1844.

(Nutt.) Britton, Mem. Torrey Bot. Club 5: 298. 1894.

USA: “Missouri”, ca. 1811, Nuttal s.n., (holotype, PH).

(A. Heller) Holub, Preslia 70: 100. 1998.

A. Heller, Bull. Torrey Bot. Club 24: 313. 1896.

Beck, Pflanzenr. 96[IV,261]: 49. 1930.

(A. Heller) Achey, Bull. Torrey Bot. Club 60: 445. 1933.

USA: Idaho: Nez Perce Co.: near mouth of the Potlatch, 20 May 1896, Heller 3099. (no holotype designated; isotypes, CAS, DAO, K, MIN, MO, MSC, NDG, PH, US).

(L.) Torr & A. Gray, Manual (Gray) 290. 1848

L., Sp. Pl. 2: 633. 1753.

(L.) Endl., Gen. Pl. [Endlicher] 727. 1839.

(L.) Britton,

Type locality.

USA: Virginia (lectotype, Clayton 387, BM).

A. Gray, Bot. California [W.H. Brewer] 1: 584. 1876

Phil., Linnea 29: 36. 1858. [Type:

Beck, Bibliotheca Botanica 4(19): 78. 1890.

(A. Gray) Heckard, Madroño 22: 41. 1973.

(Cham. & Schltdl.) A. Gray, lectotype designated by Heckard, Madroño 22: 41. 1973.

Stems clearly rising above ground. Pedicels equal to or shorter than flower. Bracteoles subtending the calyx 1 or 2.

(L.T. Collins) A.C. Schneid. comb. nov.

urn:lsid:ipni.org:names:77158997-1

L.T. Collins,

USA: Arizona, Coconino Co.: near Tuba City, 1539 m, 27 September 1935, Kearney & Peebles 12867 (holotype, ARIZ; isotype, US).

(Cham. & Schltdl.) A. Gray, Bot. California 1: 584. 1876.

Cham. & Schltdl.,

(Cham. & Schltdl.) G. Don,

(Cham. & Schltdl.) Rydb.,

USA: California: Near Port of San Francisco, Aug 1816, Chamisso s.n (holotype, LE).

(Heckard) A.C. Schneid. comb. nov.

urn:lsid:ipni.org:names:77159010-1

Heckard,

USA: California: San Luis Obispo Co.: Yaro Creek, 25 May 1955, Bacigalupi, Ferris & Robbins 5242 (holotype, JEPS; isotypes, NY, RSA, US, WTU).

(Munz) A.C. Schneid. comb. nov.

urn:lsid:ipni.org:names:77159005-1

Munz,

(Munz) Heckard,

USA: California: San Bernardino Co.: Baldwin Lake, 2 June 1924, Munz 8177 (holotype, POM).

(Heckard) A.C. Schneid. comb. nov.

urn:lsid:ipni.org:names:77159011-1

Heckard,

USA: California: Santa Barbara Co.: dunes at Surf, 22 July 1954, H. M. Pollard (holotype, UC; isotype, CAS).

(Beck) A.C. Schneid. comb. nov.

urn:lsid:ipni.org:names:77159006-1

Beck,

(Beck) Rydb.,

(Beck) Heckard,

USA: Oregon: banks of the Columbia River, 1825, Douglas s.n. (lectotype, K).

(Munz) A.C. Schneid. comb. nov.

urn:lsid:ipni.org:names:77159007-1

Munz,

(Munz) Heckard,

USA: California: Colusa Co.: Princeton, October 1905, H. P. Chandler s.n. (holotype: POM, isotype: UC).

(Phil.) A.C. Schneid. comb. nov.

urn:lsid:ipni.org:names:77158998-1

Phil.,

(Phil.) Beck,

A. Gray, Proc. Amer. Acad. Arts 20: 307. 1885.

(A. Gray) Beck, Biblioth. Bot. 4(Heft 19): 81. 1890.

(A. Gray) A. Heller, Cat. N. Amer. Pl. 7. 1898.

(A. Gray) Rydb.

USA: Arizona: Fort Mojave (lectotype designated by Munz, Bull. Torrey Bot. Club 57: 620-21, Cooper s.n. in 1860-61, GH).

(Munz) A.C. Schneid. comb. nov.

urn:lsid:ipni.org:names:77159008-1

Munz,

(Munz) L.T. Collins,

USA: California: Riverside Co.: Colorado Desert, 22 April 1922, Munz & Keck 4960 (holotype: POM, isotype, US).

(Munz) A.C. Schneid. comb. nov.

urn:lsid:ipni.org:names:77159009-1

Munz,

(Munz) L.T. Collins,

Mexico, Durango, April-November 1896, Palmer 7 (holotype: GH, isotypes, MO, UC).

(Rydb.) A.C. Schneid. comb. nov.

urn:lsid:ipni.org:names:77158999-1

Rydb.,

(Rydb.) Ferris,

USA: Reynold’s Creek, 2 July 1892, Isabel Mulford s.n. (holotype, NY; isotype, MO).

(Heckard) A.C. Schneid. comb. nov.

urn:lsid:ipni.org:names:77159012-1

Heckard,

USA: Washington: Grant Co.: O’Sullivan Dam, 11 July 1950, S. W. Harris 97 (holotype, WS).

S. Watson, Proc. Amer. Acad. Arts 18: 132. 1883.

(S. Watson) Munz, Bull. Torrey Bot. Club 57: 613, t. 38, f. 3. 1931.

Mexico: Gueanajatao, Dugès s.n. (holotype, GH).

(Nutt) A. Gray. Bot. California [W.H.Brewer] 1. 585.

Nutt. Gen. N. Amer. Pl. 2: 58–59. 1818.

(Nutt) Walp. Repert. Bot. Syst. 3: 461. 1844.

(Nutt) Rydb. Fl. S.E. U.S 1338. 1903.

USA: Fort Mandan, 1810-1811, Nuttall s.n. (holotype, PH).

(Nutt) A. Gray. Bot. California [W.H.Brewer] 1. 585.

Nutt., J. Acad. Nat. Sci. Philadelphia, ser. 2 1: 179. 1848.

USA: Rio Grande, 1845, Gambel s.n. (neotype designated by White & Holmes, Sida 19: 623, USA: Texas: Jim Wells Co., 19 April 1944, Lundell & Lundell 12809, LL; isoneotype, LL).

(Jeps.) A.C. Schneid. comb. nov.

urn:lsid:ipni.org:names:77159001-1

Jeps.

(Jeps.) Heckard.

USA: California: San Bernardino Co.: Bear Valley, 1894, S. B. Parish s.n. (holotype, JEPS).

(Heckard) A.C. Schneid. comb. nov.

urn:lsid:ipni.org:names:77159013-1

Heckard,

USA: California: Ventura Co.: Dutch Harbor, San Nicolas Island, 23 April 1966, Raven & Thompson 20794 (holotype, JEPS; isotypes, MO, RSA, SBBG).

(Geyer ex Hook.) A. Gray, Bot. California 1: 585. 1876.

Geyer ex Hook.,

USA: Idaho/Washington border, Geyer 445 (holotype, K).

(L.T. Collins) A.C. Schneid. comb. nov.

urn:lsid:ipni.org:names:77159002-1

L.T. Collins,

USA: Indiana, Gibson Co.: Griffin, 16 August 1931, Deam 50941 (holotype, IND; isotypes, A, F, GH, IND, MINN, WIS).

(Heckard ex Colwell & Yatsk.) A.C. Schneid. comb. nov.

urn:lsid:ipni.org:names:77159015-1

Heckard ex Colwell & Yatsk.,

USA: California: San Francisco Co.: Lands End, 13 August 1956, Robbins 3707 (holotype, JEPS; isotypes, CAS, GH, NY).

(Mattf.) A.C. Schneid. comb. nov.

urn:lsid:ipni.org:names:77159016-1

Mattf.,

Syntypes.

Peru: Tacna, 1890, Woitschach 71 (photograph of type: F); Peru: Tacna, 1833, F. J. F. Meyen s.n.

(Phil.) A.C. Schneid. comb. nov.

urn:lsid:ipni.org:names:77159003-1

Phil.,

(A. Gray) A. Gray, Bot. California 1: 585. 1876.

A. Gray,

Beck,

USA: California: Monterey Co: Gavilan Mountains, 1860-1862, Brewer 743 (holotype, GH; isotype K).

(Jeps.) A.C. Schneid. comb. nov.

urn:lsid:ipni.org:names:77159017-1

Jeps.,

(Jeps.) Munz,

USA: California: Rock Creek, San Gabriel Mountains, 2 June 1923, F. W. Peirson 7937 (holotype: JEPS, isotype: RSA).

(Heckard & L.T Collins) A.C. Schneid. comb. nov.

urn:lsid:ipni.org:names:77159018-1

Heckard & L.T Collins,

USA: California: Mendocino Co.: Impassable Rock, 14 July 1951, Donald V. Hemphill s.n. (holotype: UC).

(Jeps.) A.C. Schneid. comb. nov.

urn:lsid:ipni.org:names:77159004-1

Jeps.,

(Jeps.) Heckard,

USA: California: Santa Clara Co.: Coyote, 14 October 1914, W. L. Jepson 6196 (holotype: JEPS, isotypes: GH, MO).

(Mattf.) A.C. Schneid. comb. nov.

urn:lsid:ipni.org:names:77159019-1

Mattf.,

Peru: Camaná: Areuipa, Hafen Chala, 26 November 1915, A. Weberbauer 7185 (isotypes: GH, US).

1	Bracteoles subtending the calyx absent; pedicels much longer than flower (2-8× length); stems subterranean or rising to about ground level	Aphyllon sect. Aphyllon (syn.: Orobanche sect. Gymnocaulis)
1’	Bracteoles subtending the calyx 2; pedicels equal to or shorter than flower, occasionally 2× length; stems usually rising above ground level	Aphyllon sect. Nothaphyllon (syn.: Orobanche sect. Nothaphyllon)