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

Abstract 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 Diphelypaea Nicolson is nested within Orobanche sensu lato (s.l.) as circumscribed by Beck (1890) (Schneeweiss et al. 2004a). Morphological and cytological diff erences between groups of taxa within Orobanche s.l. have led some botanists to adopt a narrower generic circumscription. In this taxonomic concept, Orobanche 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(Holub , 1990. Other Old World broomrapes are treated as Phelipanche Pomel or the monotypic genus Boulardia F.W. Schultz (syn: O. sect. Trionychon Wallr. and O. latisquama (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 Phelipanche (Schneider et al. 2016). Taxonomically, these clades have been recognized as two separate genera Aphyllon (= Orobanche sect. Gymnocaulis Nutt.) and Myzorrhiza Phil. (= O. sect. Nothaphyllon (A. Gray) Heckard) by Holub (1977Holub ( , 1990 and others (Schneweiss 2013), or more rarely, together as Aphyllon 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 Aphyllon 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 Orobanche s.l., a maximum likelihood (ML) phylogram of Aphyllon 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). Th e ML phylogeny was estimated using RAxML (Stamatakis 2014) with a GTR+Γ nucleotide substitution model and 1000 rapid bootstrapping replicates.
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 O. weberbaueri Mattf. have been designated by previous authors and are presented here. For three of the four South American taxa, typifi cation would require more careful eff orts beyond the scope of this article. No repository is given in the protologue for two syntypes of Orobanche tacnaensis Mattf. (Woitschach 71 and F. J. F. Meyen s.n.). Th e current existence of these specimens could not be verifi ed, 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 O. sect. Gymnocaulis and O. sect. Nothaphyllon (McNeal et al. 2013;Schneider et al. 2016; Fig. 1). Th is relationship is supported by biogeography and synapomorphies such as a calyx with fi ve fully developed lobes and a base chromosome number of x = 12, with polyploidy in most   taxa (Heckard and Chuang 1975;Schneeweiss et al. 2004b). Holub (1977Holub ( , 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 Orobanche sect. Nothaphyllon is most closely related to Phelipanche and that O. sect. Gymnocaulis is allied to O. sect. Orobanche (Holub, 1977). Th e genus Aphyllon was described by Mitchell (1769), although it was not until nearly 80 years later that Asa Gray made a combination for A. unifl orum A. Gray. Th is 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 Aphyllon to taxa assignable to O. sect. Gymnocaulis, instead recognizing O. ludoviciana Nutt. in Phelipaea Tourn. ex Desf. However, after a study of the Californian fl ora, Gray amended his generic concept of Aphyllon to include two sections, Aphyllon and Nothaphyllon, together containing all taxa native to the New World (Gray 1876). Th ough expanded from Gray's initial circumscription, it was appropriate given Michell's original diagnosis of Aphyllon as having a fi ve-toothed calyx ("semiquinquefi dum"), a synapomorphy of New World broomrapes. A generation later, Rydberg (1906) proposed elevating Gray's Aphyllon sect. Nothaphyllon to genus rank on the basis of diff erences in habit and placentation using the available name Myzorrhiza Phil. However, the broader generic concept of Orobanche used by Beck (1890) has prevailed, particularly among American botanists.
Due to the biogeographical, morphological, cytological, and phylogenetic affi nities of the New World broomrapes, I recommend treating them in a single genus, Aphyllon, composed of sections Aphyllon (= O. sect. Gymnocaulis) and Nothaphyllon (= O. sect. Nothaphyllon). Below, I present a key to sections and a list of recognized taxa in Aphyllon, proposing new combinations as necessary. Combinations are made at the most recently treated rank for the taxon in Orobanche, with the exception of Orobanche unifl ora subsp. occidentale Greene, which is recognized at species rank under the available name Aphyllon purpureum (A. Heller) Holub due to its unique hosts, long molecular branch lengths, and recent discovery of sympatric populations of A. purpureum and A. unifl orum in southwestern British Columbia (Schneider et al. 2016). Th e treatment of Aphyllon sect. Aphyllon should be considered tentative; further taxonomic study is underway which will result in the recognition of several additional taxa.