classification and Phylogeny of amaRyllidaceae, the

modeRn synthesis and the Road ahead: a Review

clasificación y filogenia de amaRyllidaceae, la síntesis modeRna y

el camino PoR RecoRReR: una Revisión

Alan W. Meerow

Resumen

La clasiﬁcación y la historia ﬁlogenética de las Amaryllidaceae se revisa desde el

Arizona State University, School

amanecer de la sistemática molecular en la década de 1990. Actualmente, se

reconoce que la familia comprende tres subfamilias: Agapanthoideae, Allioideae y

Amaryllidoideae, de las cuales la última es la más grande. La familia probablemente

se originó en Gondwana, en lo que ahora es África. Agapanthoideae es monotípica,

endémica de Sudáfrica y la primera rama del árbol genealógico de la vida de la

familia; Allioidieae es hermana de Amaryllidoideae. Se reconocen cuatro tribus en

Allioideae: Allieae (monotípica, con casi 1000 especies de Allium en el hemisferio

norte), Gilliesieae (5-7 géneros del sur de América del Sur), Leucocoryneae (seis

géneros principalmente en el sur de América del Sur) y Tulbaghieae (monotípica,

con unas 30 especies endémicas de Sudáfrica). Amaryllidoideae es cosmopolita,

pero en su mayoría pantropical, y consta de 13 tribus. Los centros de diversidad

se encuentran en Sudáfrica, América del Sur y la región del Mediterráneo. El clado

americano es hermano del clado euroasiático (tribus Galantheae, Lycorideae,

Narcisseae y Pancratieae) de la subfamilia. Las Amaryllidoideae americanas se

resuelven en dos grupos monoﬁléticos, 1) el clado hippeastroide (tribus Griﬃneae

e Hippeastreae) y 2) el clado tetraploide andino (tribus Clinantheae, Eucharideae,

Eustephieae e Hymenocallideae). Se revisan los análisis moleculares para cada

clado principal de la familia, junto con los cambios taxonómicos resultantes. Se

discuten brevemente las direcciones para futuros estudios.

of Life Sciences, Tempe, AZ USA,

and Montgomery Botanical Center,

Coral Gables, FL, USA

*ameerow@asu.edu

Citar este artículo

MEEROW, A. W. 2023. Classification

and phylogeny of Amaryllidaceae,

the modern synthesis and the road

ahead: a review. Bol. Soc. Argent.

Bot. 58: 355-373.

DOI: https://doi.

org/10.31055/1851.2372.v58.

n3.40046

PalabRas clave

Geóﬁtos, monocotiledóneas, sistemática, secuencias de ADN, taxonomía.

summaRy

The classiﬁcation and phylogenetic history of the Amaryllidaceae is reviewed since

the dawn of molecular systematics in the 1990’s. The family is now recognized as

comprising three subfamilies: Agapanthoideae, Allioideae, and Amaryllidoideae, of

which the latter is the largest. The family likely had a Gondwanaland origin in what

is now Africa. Agapanthoideae is monotypic, endemic to South Africa, and the ﬁrst

branch in the family tree of life; Allioidieae is sister to Amaryllidoideae. Four tribes

are recognized in Allioideae: Allieae (monotypic, with nearly 1000 species of Allium

acrosstheNorthernHemisphere),Gilliesieae(5-7generainsouthernSouthAmerica),

Leucocoryneae (six genera mostly in southern South America), and Tulbaghieae

(monotypic, with ca. 30 species endemic to South Africa). Amaryllidoideae is

cosmopolitan, but mostly pantropical, consisting of 13 tribes. Centers of diversity

occur in South Africa, South America and the Mediterranean region. The American

clade is sister to the Eurasian clade (tribes Galantheae, Lycorideae, Narcisseae

and Pancratieae) of the subfamily. The American Amaryllidoideae resolves as two

monophyletic groups, 1) the hippeastroid clade (tribes Griﬃneae and Hippeastreae)

and 2) the Andean tetraploid clade (tribes Clinantheae, Eucharideae, Eustephieae,

and Hymenocallideae). Molecular analyses are reviewed for each main clade of the

family, along with the resultant taxonomic changes. Directions for future studies are

brieﬂy discussed.

Recibido: 27 Ene 2023

Aceptado: 7 Abr 2023

Publicado en línea: 30 Jul 2023

Publicado impreso: 30 Sep 2023

Editores: Nicolás García Berguecio

Key woRds

DNA sequences, geophytes, monocots, systematics, taxonomy.

&

Agostina B. Sassone

ISSN versión impresa 0373-580X

ISSN versión on-line 1851-2372

355

Bol. Soc. Argent. Bot. 58 (3) 2023

intRoduction

has Allioideae Herb. and Amaryllidoideae Burnett

as sister groups, and Agapanthoideae sister to both

Our understanding of angiosperm phylogeny (Baker et al., 2022).

has undergone a revolution over the past three

Basedonthecladisticrelationshipsofchloroplast

decades, largely due to two spectacular advances DNA sequences (Ito et al., 1999; Meerow et al.,

in the science of systematic botany (Judd et al., 1999) all three subfamilies originated in Africa

2

015). With the advent of polymerase chain (Gondwanaland) and infrafamilial relationships

reaction (PCR) technology (Saiki et al., 1988), are resolved along biogeographic lines (Fig. 1).

direct comparison of the nucleotide sequences Subfamily Amaryllidoideae, the largest in number

of organismal DNA became possible. Secondly, of genera, has colonized all continents except

phylogenetic analysis has become the standard Antarctica. Janssen & Bremer (2004) estimated

methodology for testing hypotheses of phylogeny the age of the family at 87 million years before

among organisms in systematic biology (Wiley, present (MYBP). The only fossil for the family

1

981; Felsenstein, 2004) based upon principles is from early Eocene western North America and

formally enumerated by Hennig (1966). To the was diagnosed as allied to Allioideae (Pigg et al.,

parsimony method (Kitching et al., 1998) has been 2018); contested by Friesen (2022). A leaf fossil

added both maximum likelihood (Huelsenbeck & from Colombia assigned by Wing et al. (2018) to

Crandall, 1995) and Bayesian analysis (Beaumont, Amaryllidaceae is at best ambiguous.

2

010), which have proven valuable in dealing with

large DNA sequence datasets.

Agapanthoideae

The precise relationship of Amaryllidaceae

The genus Agapanthus (subfamily

J.St.-Hil. to other Asparagales remained elusive Agapanthoideae) is restricted to South Africa

until Fay & Chase (1996) used the plastid gene and consists of six to 10 species of rhizomatous,

rubisco (rbcL) to argue that Agapanthus L’Hér., evergreen or deciduous perennials, most with

Alliaceae Borkh., and Amaryllidaceae form a blue ﬂowers (Snoeijer, 2004). The ﬂowers have

monophyletic group (also evident in Chase et al., superior ovaries, and the genus contains saponins.

1

995a, b), and that together they are related most To date, no molecular studies have been conducted

closely to Hyacinthaceae Batsch ex Borkh. s.s. to estimate the species phylogeny of this relatively

and the resurrected family Themidaceae Salisb. small genus.

(

the former tribe Brodiaeeae of Alliaceae), both

now classified as subfamilies within a broad Allioideae

circumscription of Asparagaceae Juss. (APG, Allioideae is represented in Africa by the

009). They recircumscribed Amaryllidaceae South African endemic genus Tulbaghia L., and

2

to include Agapanthus, previously included in a single species of Allium L., but is most diverse

Alliaceae, as subfamily Agapanthoideae Endl. generically in southern South America (Chile and

Subsequent analyses of multiple DNA sequences Argentina). Three tribes were recognized by some

from both the chloroplast and nuclear genomes (Chase et al., 2009; Escobar et al., 2020): Allieae

have shown quite strongly that Agapanthus, Dumort., Gilliesieae Baker and Tulbaghieae

Amaryllidaceae, and Alliaceae represent a distinct Endl. ex Meisn. Leucocoryneae Ravenna is now

lineage within the monocot order Asparagales accepted as a fourth distinct tribe (Sassone et

Link (Meerow et al., 1999; Fay et al., 2000), al., 2018), of which the ﬁrst and third consist of

but the exact relationships among the three only a single genus, Allium and Tulbaghia (the

groups have been diﬃcult to resolve with ﬁnality monotypic genus Prototulbaghia Vosa appears

(

Graham et al., 2006); APG II (APG, 2003) nested within Tulbaghia (Staﬀord et al., 2016)).

recommended treating all three as a single family, The subfamily is characterized by solid

Alliaceae (which had nomenclatural priority at styles, superior ovaries and the unique allyl

that time), and more emphatically in APG III sulﬁde chemistry that gives many members their

(

APG, 2009), but as Amaryllidaceae, reﬂecting the characteristic garlic odor. Monotypic Allieae is

successful proposal for superconservation of the the largest tribe, entirely due to the speciose genus

name (Meerow et al., 2007). Current consensus Allium (Friesen, 2022; Li et al., 2010).

356

A. W. Meerow - Classiﬁcation and phylogeny of Amaryllidaceae

Tulbaghieae

(Mill.) Prokh: Gurushidze et al., 2007, origins of

The South African endemic genus Tulbaghia A. ampeloprasum L. horticultural races and section

consists of 20-30 species and is badly in need Allium: Hirschegger et al., 2010). Other molecular

of a thorough taxonomic revision. Vosa (2007) phylogenetic investigations have been concerned

recognized a monotypic segregate genus with the origins of economically important Allium

Prototulbaghia that in a recent molecular study crops (e.g. Friesen & Klaas, 1998; Friesen et al.,

resolved as sister to one subclade of Tulbaghia 1999; Blattner & Friesen, 2006; Friesen, 2022).

spp. (Staﬀord et al., 2016). Vosa (2009) presented a Nguyen et al. (2008) examined the phylogeny

synoptic classiﬁcation for the genus, distinguishing of the western North American species and their

species groups (sections) primarily on the basis of adaptation to serpentine soils.

the morphology of the staminal corona, recognizing

Friesen et al.’s (2006) analysis of 195 species of

2

3 species, but Staﬀord et al. (2016) suggest that Allium using the ITS region of nrDNA presented

there may be as many as 30. Tulbaghieae is endemic a new subgeneric classiﬁcation consisting of 15

to South Africa and is sister to the South American monophyletic subgenera, and this is still mostly

tribes Gilliesieae (Costa et al., 2020; Escobar et al., accepted. Earlier, Friesen et al. (2000) showed

2

020) and Leucocoryneae (ca. six genera Sassone that the anomalous Milula Prain with a spicate

&

Giussani, 2018).

inﬂorescence was nested within the Himalayan

species of Allium. Nectaroscordum Lindl. and

Caloscordum Herb. are also retained within Allium.

Allieae

Allium contains over 900 species (Herden et Li et al. (2010) used ITS sequences along with the

al., 2016) and is one of the largest genera of intron of the plastid gene rps16 across over 300

monocots known. More than 50 species are used as Allium taxa and included a biogeographical analysis

edible, medicinal and ornamental crops. Variable of the genus. Three major clades are consistently

morphologically as well as ecologically, it has resolved (Fritsch, 2001; Fritsch & Friesen, 2002;

spread across the Holarctic region, inhabiting dry Friesen et al., 2006; Li et al., 2010), which Xie et

subtropics to boreal vegetation. Only a single al.’s (2020) whole plastome phylogeny supports

species of Allium occurs outside the Holartic zone, as well. Subgenera Amerallium, Anguinum G.Don

A. synnotia G.Don (syn. A. dregeanum Kunth), ex W.D.J.Koch) N.Friesen, Vvedenskya (Kamelin)

native to South Africa (de Wilde-Duyfjes, 1976; R.M.Fritsch, Porphyroprason (Ekberg) R.M.Fritsch

de Sarker et al., 1997), though Friesen (2022) and Melanocrommyum originated in eastern Asia.

suggests that it may have been introduced by Theputativelyoldestlineageconsistsofonlybulbous

early European colonists. An Old World center plants (subgenera Nectaroscordum, Microscordum

of diversity encompasses the Mediterranean (Maxim.) N.Friesen and Amerallium) that only

Basin to Central and Eastern Asia, with a second rarely produce a rhizome (Fritsch & Friesen, 2002).

smaller one in western North America. Friesen The second clade includes subgenera Caloscordum,

(2022), Friesen et al. (2006) and Li et al. (2010) Anguinum, Vvedenskya, Porphyroprason and

review the infrageneric taxonomic history of this Melanocrommyum, and the third subgenera

complex genus. Molecular studies have either Butomissa (Salisb.) N. Friesen, Cyathophora,

addressed the phylogenetic relationships of the Rhizirideum, Allium, Cepa, Reticulatobulbosa

entire genus (Mes et al., 1997; Dubouzet & (Kamelin) N. Friesen and Polyprason Radić. The

Shinoda, 1999; He et al., 2000; Fritsch & Friesen, latter two contain both rhizomatous and bulbous

2

002; Friesen et al., 2006; Li et al., 2010, 2016b; species. The third clade was the most poorly

Xie et al., 2020) or speciﬁc subgenera and sections resolved in these analyses and includes a number

Amerallium Traub: Samoylov et al., 1995, 1999; of non-monophyletic subgenera (Li et al., 2010),

Cyathophora (R.M.Fritsch) R.M.Fritsch: Li et but resolution and levels of support were greatly

al., 2016a Melanocrommyum (Webb & Berth.) increased with analysis of whole plastomes (Xie

Rouy: Dubouzet & Shinoda, 1998; Mes et al., et al., 2020). A scenario of rapid radiation was

1

999; Gurushidze et al., 2008, 2010; Fritsch proposed for this clade. The ﬁrst two clades contain

et al., 2010, Rhizirideum (G. Don ex Koch) both Old and New World species; almost all of the

Wendelbo: Dubouzet et al., 1997, section Cepa western North American species are classiﬁed in

357

Bol. Soc. Argent. Bot. 58 (3) 2023

subgenus Amerallium (Nguyen et al., 2008), which Gilliesia, Gethyum Phil. and Solaria Phil., and

has sparingly extended to central and eastern North Clade II, Miersia Lindl. and Speea Loes. However,

America. The only other North American species Gilliesia, Gethyum and Miersia were all found

are members of subg. Anguinum (Li et al., 2010; to be paraphyletic, resulting in the recognition of

Xie et al., 2020).

the monotypic genus Ancrumia Harv. ex Baker.

Costa et al. (2020) estimated the age of Schickendantziella Speg. and Trichlora Baker

Allioideae as ca. 63 million years and hypothesized were not represented in the sampling. García et al.

that the Indian plate rafted Allieae to the northern (2022a) resolved the same phylogenetic tree, and

hemisphere from which the genus Allium (ca. 52 published two novel species of Miersia.

MYBP) diversiﬁed via polyploidy and geographic

Sassone and colleagues have studied

spread throughout the Northern Hemisphere. Leucocoryneae extensively (Sassone & Arroyo-

Friesen (2022) supported this hypothesis.

Leuenberger, 2018; Sassone & Giussani, 2018;

Sassone et al., 2013; Sassone et al., 2018), and the

taxonomic history of the tribe is summarized in

Gilliesieae and Leucocoryneae

The tribes Gilliesieae and Leucocoryneae are Sassone & Giussani (2018).

entirely restricted to the American continents

This tribe consists of six South American genera

and are most diverse in southern South America, with ca. 100 species (Sassone et al., 2014a):

especially Argentina and Chile, and includes such Beauverdia Herter (four spp., Sassone et al.,

established ornamental bulb crops as Ipheion 2014b), Ipheion (three spp., Sassone et al., 2014a),

Raf. and Leucocoryne Lindl. Only one species of Latace Phil. (two spp., Sassone et al., 2015),

Nothoscordum Kunth extends outside of that region, Leucocoryne (15 spp., Muñoz & Moreira, 2000),

and may be adventive. The sister relationship of Nothoscordum (20-80 spp.), and Tristagma Poepp.

these tribes to Tulbaghieae (Fay & Chase, 1996; (12 spp.; Arroyo-Leuenberger & Sassone, 2016).

Fay et al., 2006) suggests an austral entry into However, both Tristagma and Nothoscordum

South America, perhaps via Antarctica, as has resolve as biphyletic (Pellicer et al., 2017; Sassone

been suggested for many groups showing a similar & Giussani, 2018), and Beauverdia, with both white

biogeographic scenario (Raven & Axelrod, 1974). and yellow uniﬂorous species, is nested within the

Unfortunately, generic limits within the group latter. For this reason, Pellicer et al. (2017) argued

remain problematic, with many species having been that Beauverdia should be placed into synonomy

variously treated as members of diverse genera with Nothoscordum. Most recently García et al.

(Rahn, 1998; Zöllner & Arriagada, 1998; Rudall et (2022b) described a new monotypic genus in the

al., 2002; Fay et al., 2006). Leucocoryneae, Atacamallium Nic.García, which

The two tribes are immediately separable resolved as sister to the genus Leucocoryne.

by the symmetry of the ﬂowers; all Gilliesieae

are zygomorphic, and all Leucocoryneae are Amaryllidoideae

actinomorphic. The latter also alone possess septal

The largest subfamily of Amaryllidaceae in

nectaries (Rudall et al., 2002). Both tribes show number of genera is Amaryllidoideae (Fig. 1). This

greater variability in karyotype than either Allium subfamily is also economically important, albeit for

or Tulbaghia (Costa et al., 2020). A combination its large number of ornamental bulbs rather than any

of plastid and ribosomal DNA sequences robustly food value. It is characterized by an inferior ovary, a

supports the two floral morphological clades unique group of alkaloidal compounds, many with

(Fay et al., 2006; Pellicer et al., 2017; Sassone & bioactive properties (Meerow & Snijman, 1998; He

Giussani, 2018). Interestingly, the zygomorphic et al., 2015), and base chromosome number of x =

ﬂowers of Gilliesia Lindl. are hypothesized to be 11 (Meerow & Snijman, 1998).

insect mimics with a pseudocopulatory pollination

Tribe Amaryllideae, entirely southern African

syndrome (Rudall et al., 2002).

with the exception of pantropical Crinum L., is

Escobar et al. (2020) applied ITS and plastid sister to the rest of Amaryllidaceae with very high

rbcL and trnL-F sequences to explore generic bootstrap support in Meerow et al.’s (1999) analysis

limits in the Gilliesieae. Two major clades were of plastid genes (Fig. 1). The remaining two African

well-supported: Clade I comprises the genera tribes of the family, Haemantheae Hutch. (including

358

A. W. Meerow - Classiﬁcation and phylogeny of Amaryllidaceae

subtr. Gethyllidinae Dumort) and Cyrtantheae Strumariinae sensu D. & U. Müller-Doblies [1985,

Traub (consisting of only Cyrtanthus Ait.), were 1996]). Meerow & Snijman (2001) analyzed

well supported, but their position relative to the morphology and ITS sequences across the entire

Australasian Calostemmateae D.Müll.-Doblies & tribe. Amaryllis is sister to the remaining genera,

U.Müll.Doblies and a large clade comprising the followed by Boophone. All other genera were

Eurasian and American genera, was not clear. Most included in two clades conforming to Snijman

surprising, the Eurasian and American elements of & Linder’s (1996) subtribes Amaryllidinae (less

the family were each monophyletic sister clades. Amaryllis, thus now Strumariinae) and Crininae

Ito et al. (1999) resolved a very similar topology (less Boophone), and Carpolyza was transferred

for a more limited sampling of Amaryllidaceae and into Strumaria (Meerow & Snijman, 2001).

related asparagoids using plastid matK sequences.

Plastid ndhF sequences (Meerow & Snijman, biogeographical analyses of nrDNA ITS and plastid

006) resolved Cyrtantheae as sister to a clade of trnL-F sequences for all continental groups of the

Meerow et al. (2003) presented phylogenetic and

2

Calostemmataeae and Haemantheae.

large, pantropical genus Crinum and related genera.

Their results indicated that C. baumii Harms is

more closely related to Ammocharis than to Crinum

Amaryllideae

Almost all of the generic diversity of the tribe sensu stricto (s.s.). Three clades are resolved in

Amaryllideae is conﬁned to South Africa (Snijman Crinum s.s. The ﬁrst one unites a monophyletic

&

Linder, 1996). Compared to other tribes in American group with tropical and North African

Amaryllidaceae, Amaryllideae is marked by a large species. Meerow et al. (2003) hypothesized that

number of synapomorphies (Snijman & Linder, emergent aquatic tropical African species with

1

996; Meerow & Snijman, 1998): extensible ﬁbers actinomorphic perianths were likely the sister group

in the bulb tunics, bisulculate pollen with spinulose to the American species, which was shown to be

exine, scapes with a sclerenchymatous sheath, the case by Kwembeya et al. (2007). The second

unitegmic or ategmic ovules, and nondormant, clade included all southern African species and the

water-rich, nonphytomelaninous seeds with Australian endemic C. ﬂaccidum Herb. The third

chlorophyllous embryos. A few of the genera includes monophyletic Madagascar, Australasian

extend outside of South Africa proper, but only and Sino-Himalayan clades, with southern African

Crinum, with seeds well suited to oceanic dispersal species. The salverform, actinomorphic perianths of

(Koshimizu, 1930), ranges through Asia, Australia, subg. Crinum appear to have evolved several times

and America. The tribe is the ﬁrst branch within the in the genus from ancestors with zygomorphic

subfamily (Ito et al., 1999; Meerow, 2010; Meerow perianths (subg. Codonocrinum Willd. ex

et al., 2000; Meerow & Snijman, 2006). Snijman and Schult.f.), thus neither subgenus is monophyletic.

Linder’s (1996) phylogenetic analysis of the tribe Biogeographical analyses place the origin of

based on morphological, ﬂoral and seed anatomical, Crinum in southern Africa. The genus underwent

and cytological data resulted in recognition of three major waves of radiation corresponding to

two monophyletic subtribes: Crininae Baker the three main clades resolved in the trees. Two

(Boophone Herb., Crinum, Ammocharis Herb., and entries into Australia of the genus were indicated,

Cybistetes Milne-Redh. & Schweick., the latter now as were separate Sino-Himalayan and Australasian

transferred to Ammocharis (Snijman & Williamson, dispersal events. These results were conﬁrmed by

1

994) and Amaryllidinae Walp. (Amaryllis L., Kwembeya et al. (2007), including the origin of

Nerine Herb., Brunsvigia Heist., Crossyne Salisb., the endemic American species from tropical west

Hessea Herb., Strumaria Jacq., and Carpolyza African spp.

Salisb. Carpolyza has been transferred to Strumaria

(Meerow & Snijman, 2001). Meerow et al.’s (1999) Calostemmateae, Cyrtantheae and Haemantheae

incomplete sampling of this tribe for three plastid The three tribes Calostemmateae, Cyrtantheae

sequences resolved Amaryllis as sister to the rest and Haemantheae form a clade that is sister to the

of the tribe. Weichhardt-Kulessa et al. (2000) American and Eurasian tribes of the subfamily

presented an analysis of internal transcribed spacer (Fig. 1; Meerow et al., 1999; Meerow & Snijman,

(ITS) sequences for a part of the tribe (subtribe 2006), though their exact relationships to each other

359

Bol. Soc. Argent. Bot. 58 (3) 2023

remain ambiguous (Meerow & Snijman, 2006; The Eurasian clade (Lycorideae, Galantheae,

Bay-Schmidt et al., 2010).

Narcisseae, and Pancratieae)

Calostemmateae consists of two Australasian

The Eurasian clade of the Amaryllidaceae (Fig.

genera (Proiphys Herb., pseudopetiolate forest 1) contains the members of the family that have

understory herbs of Malaysia, Indonesia, the adapted to the highest latitudes in the Northern

Philippines and tropical Australia; and Calostemma Hemisphere, and also those with the greatest

R. Br., endemic to Australia). The indehiscent economic value as spring flowering temperate

capsules of both genera are similar in appearance zone garden plants (Narcissus L., Galanthus

to the unripe berry-fruits of Scadoxus Raf. and L., Leucojum L.). The clade was only recently

Haemanthus L. (Haemantheae), but early in the recognized as a monophyletic group, resolved as

development of the seed, the embryo germinates sister to the endemic American genera by plastid

precociously, and a bulbil forms within the capsule DNA sequences (Ito et al., 1999; Meerow et al.,

and functions as the mature propagule (Rendle, 1999). The Eurasian clade encompasses four

1

901). A reasonable hypothesis is that the lineage tribes that were previously recognized (Meerow

represents an early entry into Australia directly & Snijman, 1998): Galantheae Parl., Lycorideae

from Africa. Herb., Narcisseae Lam. & DC., and Pancratieae

Cyrtantheae consists of a single genus. Dumort., the overall relationships of which were

Cyrtanthus is endemic to sub-Saharan Africa, with obscured by their diversity of chromosome number

well over 90% of its species concentrated in South and morphology (Traub, 1963). Müller-Doblies &

Africa (Dyer, 1939; Reid & Dyer, 1984). With Müller-Doblies (1978a) earlier observed similarities

about 55 species it is the largest genus of southern between the internal bulb morphology of Ungernia

Africa’s Amaryllidaceae (Snijman & Archer, Bunge (Lycorideae) and Sternbergia Waldst. & Kit.

2

003) and one of the largest in the family overall (Narcisseae). With the exception of the Central and

(

Snijman & Meerow, 2010). The genus exhibits a East Asian Lycorideae, the clade is centered within

high level of ﬂoral morphological diversity which the Mediterranean region (Meerow & Snijman,

is unparalleled in any other genus of the family. 1998; Lledó et al., 2004). There are 11 genera in the

Conversely, the genus shows great consistency in clade, comprising ca. 120 spp., with Lycoris Herb.

chromosome number, with 2n = 16 characteristic (ca. 20 spp.) and Narcissus L. (40 spp.) the largest

of most, if not all, of the species (Wilsenach, genera (Meerow & Snijman, 1998).

1

963; Ising, 1970; Strydom et al., 2007). It is

Lledó et al. (2004) presented a cladistic analysis

also the only African genus with the ﬂattened, of the clade that focused on the relationships of

winged, phytomelaninous seed, so common in the Leucojum and Galanthus using plastid matK,

American clade of the family (Meerow & Snijman, nuclear ribosomal ITS sequences, and morphology.

1

998). Snijman & Meerow (2010) explored the Leucojum was revealed as paraphyletic, and the

phylogeny of the genus in the context of ﬂoral genus Acis Salisb. was resurrected to accommodate

and ecological adaptation using plastid ndhF and the linear-leaved Mediterranean Leucojum species

nuclear ribosomal DNA.

with solid scapes. While their sampling within these

Haemantheae is the only group of three genera was extensive, only a single species

Amaryllidaceae that have evolved a baccate fruit each of the genera Pancratium L., Sternbergia,

(

Meerow et al., 1999; Meerow & Clayton, 2004). It Narcissus, and Vagaria Herb., along with the

is entirely African, and like Cyrtanthus, most of its monotypic Lapiedra Lag., were used as outgroups.

diversity is in South Africa (Meerow & Snijman, Hannonia Braun-Blanq. & Maire was not included.

1

998). Meerow & Clayton (2004) analyzed plastid Consequently, the phylogenetic relationships of

trnL-F and nrDNA ITS sequences across the tribe. the entire clade were not explicitly examined in

Two main clades are resolved, one comprising the their analyses. A similar case holds for Graham

monophyletic rhizomatous genera Clivia Lindl. & Barrett’s (2004) study of ﬂoral evolution in

and Cryptostephanus Welw. ex Baker, and a Narcissus using plastid ndhF and trnL-F sequences,

larger clade that unites Haemanthus and Scadoxus which included only Lapiedra and one species

as sister to an Apodolirion Baker/Gethyllis L. each of Galanthus, Leucojum, and Sternbergia as

subclade.

outgroups in their analyses.

360

A. W. Meerow - Classiﬁcation and phylogeny of Amaryllidaceae

Meerow et al. (2006) analyzed the clade using x = 7. He recognized 10 sections (Apodanthae [as

plastid ndhF and rDNAITS sequences for 33 and 29 Apodanthi] A. Fernandes, Aurelia (J. Gay) Baker,

taxa, respectively; all genera were represented by at Bulbocodii DC., Ganymedes (Haw.) Schult f.,

least one species. Both sequence matrices resolve Jonquilla DC., Narcissus, Pseudonarcissus DC.,

the Central and East Asian tribe Lycorideae as sister Serotini Parl., Tapeinanthus (Herb.) Traub and

to the Mediterranean-centered genera of the clade, Tazettae DC.) based on his decades of karyotypic

and two large subclades were recognized within studies in the genus (summarized in Fernandes,

the greater Mediterranean region: Galantheae, 1967, 1968a, b, 1975). Pérez-Barrales et al.,

consisting of Acis, Galanthus and Leucojum; (2003) used the short plastid intergenic spacer

and Narcisseae (sister genera Narcissus and between trnL and trnF across a small sampling of

Sternbergia, and Pancratium). However, there were Narcissus species and did not get much resolution

areas of incongruence between the two markers, beyond the two recognized subgenera. Graham

which disappeared when three predominantly & Barrett (2004) provided phylogenetic analyses

monotypic genera, Hannonia, Lapiedra, and of the plastid trnL-F and ndhF regions sequenced

Vagaria, centered in North Africa, were removed from 32 Narcissus species representing all 10

from the alignments. The authors hypothesized sections recognized by Fernandes (1975) and

that incomplete lineage sorting took place after Blanchard (1990). This report strongly supported

the divergence of Galantheae and Narcisseae/ monophyletic subgenera Hermione and Narcissus,

Pancratium from a common ancestor, with the three but not of all sections. Only section Apodanthae

small or monotypic genera retaining a mosaic of the was clearly monophyletic, but several clades

ancestral haplotypes. After the vicariant divergence corresponded approximately to recognized sections

of the Asian Lycorideae, North Africa and the (Graham & Barrett, 2004). The most robust study is

Iberian Peninsula are the most likely areas of origin that of Marques et al. (2017) who utilized plastid,

for the rest of the clade (Meerow et al., 2006). A mitochondrial and nrDNA (ITS) across a large

new genus, Shoubiaonia W.H.Qin, W.Q.Meng & sampling of species with multiple accessions. She

Kun Liu, was recently described in Lycorideae and uncovered striking incongruence between trees

is sister to Lycoris and Ungernia (Qin et al., 2021).

supported by the cytoplasmic versus the nuclear

Narcissus is the most important genus of sequences, which she attributed to widescale

temperate zone spring flowering bulbs in the hybridization throughout the evolutionary history

Amaryllidaceae. The genus is taxonomically very of the genus. Tests for recombination in the ITS

complex (Fernandes, 1968a; Webb, 1980; Mathew, alignments supported this hypothesis. Again, only

2

002), no doubt in part due to its propensity to few of Fernandes’ (1968a) sections were found to

hybridize in nature (Marques, 2010), and the many be monophyletic. Könyves et al. (2019) concluded

horticultural hybrids and selections (Mathew, much the same in their study of Narcissus section

2

002). Consequently, the number of species varies Bulbocodii.

considerably in diﬀerent studies. For example, The sister genus to Narcissus is Sternbergia

Webb (1980) recognized 26 species; Fernandes (Meerow et al., 2006), a small genus of ca.

1968a) accepted 63. Blanchard (1990) favored eight dwarf white or yellow cup-shaped ﬂowered

(

Fernandes’ (1968a) treatment. The genus is most species, generally appearing in autumn. The

speciose in the Western Mediterranean area, scapes are uniﬂorous. It is distributed around the

particularly the Iberian Peninsula and NW Africa. Mediterranean basin, with diversity and endemism

This group is also fascinating biologically due highest from Greece to Israel. Two species ﬂower in

to the occurrence of all four major classes of spring: S. vernalis (Mill.) Gorer & J.H.Harvey and

heterostyly, from stylar monomorphism, stigma- S. candida B.Mathew. & T.Baytop, the latter the

height dimorphism, distyly, to tristyly (reviewed in sole white-ﬂowered species. S. lutea (L.) Ker Gawl.

Barrett & Harder, 2005). It is the only heterostylous ex. Spreng. has been in cultivation for millennia

genus of Amaryllidaceae.

and has naturalized in areas of northern Europe

Fernandes (1968a) divided Narcissus into two (Mathew, 1983).

subgenera, Hermione (Salisb. ex Haw.) Spach with

Gage et al. (2011) published the most recent

base chromosome number x = 5, and Narcissus with phylogeny of the genus and concluded that it forms

361

Bol. Soc. Argent. Bot. 58 (3) 2023

two main clades: 1) S. colchiciﬂora Waldst. & Kit. to Turkey and eastern Caucasus. It diﬀers from L.

sister to S. vernalis, S. candida and S. clusiana vernum by its water-dispersed seed with a dark testa

Boiss., and 2) S. lutea and its allies. The two spring and lack of elaiosomes.

ﬂowering species are closely related. In the S.

The remaining Leucojum species are now

lutea complex, there was insuﬃcient resolution, classiﬁed in the genus Acis, divided into subgenus

supporting arguments that S. sicula Tineo ex Acis or Ruminia Parl. (Lledó et al., 2004; Meerow

Guss. and S. greuteriana Kamari & R.Artelari are et al., 2006, Larsen et al., 2010), characterized by

conspeciﬁc with S. lutea.

solid scapes, narrow leaves and ﬁliform styles. The

The relationship between Galanthus subgenera Acis and Ruminia are diﬀerentiated by

and Leucojum sensu lato (s.l.) has long been the morphology of the epigynous staminal disc,

recognized, as has their relationship to Narcissus six-lobed in A. subgenus Ruminia, and unlobed in

and Sternbergia (Müller-Doblies & Müller-Doblies, A. subgenus Acis. Acis subg. Acis is the larger of the

1

978b; Davis, 1999; 2001). Both genera share two subgenera with ﬁve species.

pendulous, predominantly white ﬂowers, similar

internal bulb morphology and poricidal anthers The American clade

(

Müller-Doblies & Müller-Doblies, 1978b). Unlike

Narcissus, both lack a ﬂoral tube or a paraperigone endemic American genera (the entry of Crinum

corona). Galanthus is marked by the striking onto the continent is considered a separate event)

In the American clade, the relationships of the

(

length diﬀerences between the inner and outer tepal were well resolved using the spacer regions of

series, which are only subequal in Leucojum and nuclear ribosomal DNA(Meerow et al., 2000a), and

Acis (Meerow & Snijman, 1998).

the major relationships have also been supported by

Galanthus consists of 18 species, mostly plastid genes and introns (Meerow et al., 1999;

distributed in Europe, Asia Minor and the Near 2000b; Meerow & Snijman, 2006; Meerow, 2010).

East (Davis, 1999, 2001). Stern (1956) recognized The American genera of the family form two major

three series in Galanthus, erected primarily by subclades (Fig. 1). The ﬁrst, or hippeastroid clade,

leaf vernation: Nivales Beck (leaves ﬂat), Plicati are diploid (2n = 22), primarily the extra-Andean

Beck (leaves plicate) and Latifolii Stern (leaves element of the family (though several of the genera

convolute). Davis (1999) combined series Nivales do have Andean representatives), comprising

and Plicati into series Galanthus, and divided the Brazilian endemic tribe Griﬃnieae Ravenna

series Latifolii into two subseries: Glaucaefolii (Cearanthes Ravenna, Griﬃnia Ker Gawl. and

(

Kem.-Nath.) A. P. Davis and Viridifolii (Kem.- Worsleya (Watson ex Traub) Traub) sister to genera

Nath.) A.P.Davis. Molecular phylogenetic studies treated as tribe Hippeastreae Herb. ex Sweet in

Lledó et al., 2004; Larsen et al., 2010; Rønsted most recent classiﬁcations (Dahlgren et al. 1985;

et al., 2013) indicate that the two subseries are not Muller-Doblies & Muller-Doblies, 1996; Meerow

monophyletic. & Snijman, 1998; García et al., 2019). ITS resolved

(

Leucojum s.l. originally contained 10 species monotypic Worsleya as the ﬁrst branch in the

Stern, 1956), mostly occurring in the western tribe, and monotypic Cearanthes and Griﬃnia

(

Mediterranean area, from the Atlantic coast of (16 species) as sister genera (Campos-Rocha et

Portugal and Morocco to the northern Balkans and al., 2022b). A monograph of the tribe is underway

Crimea, but today the genus comprises only two: (Campos-Rocha et al., 2018, 2019a, b).

L. vernum L. and L. aestivum L. (Lledó et al., 2004;

Several genera within the hippeastroid clade

Meerow et al., 2006; Larsen et al., 2010), both resolved as polyphyletic (Rhodophiala C. Presl.,

broadly distributed in central and northern Europe, Zephyranthes Herb.) and the possibility of

Turkey and the Caucasus. Leucojum is characterized reticulate evolution (i.e., early hybridization) in

by hollow scapes, broad leaves and clavate styles. these lineages was hypothesized (Meerow et

Both species have a base chromosome number of x al., 2000; Meerow, 2010). This was conﬁrmed

=

11. L. vernum, the type of the genus, is widespread with further analyses of plastome and multiple

in central and northern Europe. Its seeds have a pale nuclear gene sequences (García et al., 2014, 2017).

outer testa and elaiosomes. L. aestivum is found Hippeastreae constitutes two main clades, the

throughout the Mediterranean and central Europe subtribe HippeastrinaeWalp. and the mostly Chilean

362

A. W. Meerow - Classiﬁcation and phylogeny of Amaryllidaceae

endemic subtribe Traubiinae D. Müll.-Doblies & 2017), using whole plastomes and multiple nuclear

U. Müll.-Doblies (García et al., 2014, 2017). In genes on a larger sampling of species, conﬁrmed

contrast to the Hippeastrinae, the Traubiinae exhibit this. Hippeastrum reticulatum Herb., with unusual

a mostly tree-like pattern of evolution (García et fruit and seed morphology was sister to all other

al., 2017). García et al. (2019) presented a new species of subg. Hippeastrum, recently displaced

classiﬁcation scheme for Hippeastreae that reﬂects by the morphologically unusual H. velloziﬂorum

its reticulate phylogeny. Within Hippeastriinae, Campos-Rocha & Meerow (Campos-Rocha et al.,

only two genera are recognized, Hippeastrum 2022b). The low rates of base substitution in both

Herb. (two subgenera, H. subg. Hippeastrum and plastid and nrDNA sequences, and the consistent

H. subg. Tocantinia (Ravenna) Nic.García) and interfertility of species -well-mined by bulb

Zephyranthes (five subgenera, Z. subg. Eithea breeders (Meerow, 2009)- suggest that the genus

(Ravenna) Nic.García, Z. subg. Habranthus (Herb.) underwent a relatively recent radiation (Oliveira,

Nic.García, Z. subg. Myostemma (Salisb.) Nic. 2012). Many of the species seem to intergrade with

García (= core Rhodophiala clade), Z. subg. one another. Traub & Moldenke (1949) attempted

Neorhodophiala Nic.García & Meerow subg. a formal subgeneric classiﬁcation of the genus

nov., and Z. subg. Zephyranthes). One species, Z. (as Amaryllis) based on ﬂoral morphology, but

pedunculosa (Herb.) Nic.García & S.C.Arroyo, was most of their infrageneric taxa do not appear to

designated as incertae sedis.

be monophyletic (Meerow & Snijman, 1998). The

In the second subtribe, Traubiinae, García et al. newly described H. velloziﬂorum resolves with ITS

2019) and García & Meerow (2020) recognized as sister to the rest of subgenus Hippeastrum. Lara

(

four genera, the first two monotypic Traubia et al. (2021) presented a revision of the Bolivian

Moldenke and Paposoa Nic.García, Phycella Lindl. species, recognizing 34 native to that country,

(including Placea Miers), 12 or more species all but but there was no attempt to place the taxa into a

one endemic to Chile, and the alpine Rhodolirium phylogenetic context. Oliveira (2012) recognized

Phil. with two spp., both found in Chile and 27 species (now 35) as occurring in Brazil and

adjacent Argentina. There has been a great deal of documented with sequence data and network

cytogenetic work for the subtribe (Baeza & Macaya, analysis signiﬁcant reticulation. New Brazilian

2

020; Baeza et al., 2009a, 2009b, 2012, 2017).

The economically most important genus 2013, 2017; Campos-Rocha et al., 2022a, 2022b).

of American Amaryllidaceae subfam. The second clade of the American

species continue to be described (Oliveira et al.,

Amaryllidoideae, Hippeastrum, is still not very Amaryllidoideae constitutes the tetraploid-derived

well understood taxonomically. Hippeastrum (x = 23) Andean-centered tribes (Fig. 1). All,

consists of 70-100 entirely New World species, or at least some, members of each tribe have

though one species, H. reginae Herb. appears 2n = 46 chromosomes. The Andean clade is

to have been introduced to Africa. No modern characterized by three consistent deletions, two

revision of the genus has appeared since that in the ITS1 and one in the ITS2 regions (Meerow

of Traub & Moldenke (1949). The species are et al., 2000a), with the exception of Eustephieae

concentrated in two main areas of diversity, one Hutch. which lacks the indel in ITS2. The ﬁrst

in eastern Brazil, and the other in the central branch of the clade is the tribe Eustephieae. The

southern Andes of Peru, Bolivia, and Argentina, tribes Hymenocallideae Small and its sister tribe

on the eastern slopes and adjacent foothills. A Clinantheae Meerow were recognized. A petiolate-

few species extend north to Mexico and the West leafed Andean subclade, containing elements of

Indies. Meerow et al. (2000a) included seven both Eucharideae Hutch. and Stenomesseae Traub

species in their molecular phylogenetic analysis of (tribe Eucharideae) was also resolved. Interestingly,

the American genera of subfam. Amaryllidoideae, in both of the American subclades there is a small

representative of the biogeographic range of the but diverse tribe that is sister to the rest of the

genus. Their results suggested that the genus is group, the Eustephieae in the Andean clade, and

robustly monophyletic and originated in Brazil. the Griﬃnieae in the hippeastroid clade (Fig. 1).

Campos-Rocha et al. (2022b), using 20 spp., These two small tribes likely represent very isolated

further supported these results. García et al. (2014; elements of their respective clades. Meerow (2010)

363

Bol. Soc. Argent. Bot. 58 (3) 2023

concluded that the genus Pyrolirion Herb. was the has been no other application of next generation

ﬁrst branch of the Eustephieae, rather than allied DNA technology such as sequence capture using

with Zephyranthes. Most recently, Meerow et al. anchored hybrid enrichment, also known as Hyb-

(2020) performed a phylogenomic analysis of the Seq (Cronn et al., 2012; Lemmon et al., 2012;

clade and applied a curated suite of 524 nuclear Lemmon & Lemmon, 2013; Weitemier et al., 2014)

genes and a partial plastome, which yielded well- applied to the family. Sassone et al. (2021) did

supported, fully resolved trees, with much improved apply genotyping by sequencing (GBS) to study

species resolution. All of Meerow et al. (2000)’s the diversiﬁcation of genus Ipheion in the Pampean

tribes were robustly supported as were most region as well as to investigate the domestication

genera, and their generic composition is as follows: history of Iphieon uniflorum (Graham) Raf.

Clinantheae: Clinanthus Herb., Pamianthe Stapf, (Sassone et al., 2022). Hyb-Seq is clearly the future

Paramongaia Velarde); Eucharideae: Eucrosia Ker for developing more robust phylogenetic data sets

Gawl., Phaedranassa Herb., Plagiolirion Baker, at the species and generic levels.

Rauhia Traub, Stenomesson Herb. and Urceolina

There has been interest in whole plastome

Reichb. (including Eucharis Planch. & Lind., data recently (Cheng et al., 2022; Dennehy et

Caliphruria Herb. and Eucrosia dodsonii Meerow al., 2021; Jimenez et al., 2020; Xie et al., 2020).

&

Dehgan); Eustephieae: Chlidanthus Herb., Whole plastome sequence data has been applied

Eustephia Cav., Hieronymiella Pax, Pyrolirion); to recognize new species and estimate phylogeny

and Hymenocallideae (Hymenocallis Salisb., in Lycoris (Lou et al., 2022; Zhang et al., 2021;

Ismene Salisb., Leptochiton Sealy).

Zhang et al., 2022) without any nuclear sequence

The Eustephieae, with a southerly bias in data for tree comparison. There is frequently

distribution, is always resolved as sister sizable cytonuclear discordance between phylogeny

to the rest of the clade. The monotypic genus estimates from plastome versus nuclear data in the

Androstephanos Fern.Casas, placed under family (Marques et al., 2017; García et al., 2017;

synonomy of Hieronymiella argentina (Pax) Hunz. Meerow et al., 2020), which can at times signify

&

S.C.Arroyo, appears more closely related to reticulation. To that end, one must exercise some

Eustephia with ITS sequences (unpubl. data). caution in formalizing taxonomic inferences from

Clinantheae and Hymenocallideae are sister tribes, plastomes alone, without corresponding trees from

in turn sister to the Eucharideae (Fig. 1).

the nuclear genome, especially in genera where

Unlike the Hippeastreae, the Andean clade does hybridization has been documented.

not appear to have experienced much reticulate

Evolutionary development (evo-devo) compares

evolution at the generic level (Meerow et al., 2020), the developmental processes of diﬀerent organisms

but interspeciﬁc hybridization was evident within to infer how such evolved, using molecular data

Hymenocallis especially, and within the rain forest generally of candidate genes that are integral to

understory subclade of the pseudo-petiolate leafed developmental pathways (Goodman & Coughlin,

tribe Eucharideae. As a result, Traub’s (1971) 2000) or via transcriptome data (Roux et al., 2015).

transfer of Eucharis and Caliphruria into Urceolina Very few evo-devo studies have been conducted in

was accepted (Meerow et al., 2020). Stenomesson is Amaryllidaceae (see Waters et al., 2013). Given the

its sister genus. The Peruvian endemic Caliphruria degree of canalized and convergent morphological

korsakoﬃi was transferred into Stenomesson, and characters in the family (Meerow, 2010), it is an

Eucrosia dodsonii to Urceolina (Meerow et al., approach that will hopefully see greater application

2

023).

in the future.

A ﬁnal classiﬁcation for the genera of tribes

Gilliesiae and Leucocoryneae seems within reach,

The Road Ahead

The past quarter century has resulted in the most and just requires acceptance of only monophyletic

resolute and accurate understanding of phylogenetic genera, which will then require either taxonomic

relationships in Amaryllidaceae to date. However, lumping or splitting.

despite such progress, there are still many questions

The large genera Hippeastrum and Zephyranthes

that remain to be answered. Surprisingly, outside of would beneﬁt from a next generation sequencing

García et al. (2017) and Meerow et al. (2020), there approach combined with whole plastome sequences

364

A. W. Meerow - Classiﬁcation and phylogeny of Amaryllidaceae

to unwind the obvious history of hybridization, been described from India (Sasikala & Kumari,

aneuploidy and polyploidy. In the Andean clade, 2013; Sadasivaiah, 2018).

wider sampling within Eustephieae would be

Many amaryllids are relatively rare in nature

helpful. Among the Eurasian genera, the broadly and may not ﬂower every year. New exploration

distributed Pancratium is badly in need of a will undoubtedly continue to uncover new species.

comprehensive revision as well as a well-sampled I look forward to seeing the next generation of

molecular phylogeny. New species have recently systematists working on the family.

Fig. 1. Subfamilial and tribal level phylogeny of the Amaryllidaceae, based on García et al. 2014, 2017,

2019, 2022a), Meerow (2010), Meerow & Snijman (2006), Meerow et al. (1999, 2000a, b, 2006, 2020), and

Sassone & Giussani (2018).

acKnowledgements

grants to the author. Antonio Campos-Rocha,

Asunción Cano, Norton Cuba, Julie Dutilh,

Fieldwork in South America was supported by Boris Esquerre, Nicolás García, Segundo Leiva,

USDA, and various National Science Foundation Blanca Léon, Nora Oleas, Agostina Sassone and

365

Bol. Soc. Argent. Bot. 58 (3) 2023

Deirdre Snijman at various times stimulated useful

discussions on Amaryllidaceae. I am also grateful to

the two reviewers of the manuscript, both of whom

helped improve it.

(Narcissus ). New Phytol . 165: 45-53.

https://doi.org/10.1111/j.1469-8137.2004.01183.x

BAY-SMIDT, M. G. K., A. K. JÄGER, K.

KRYDSFELDT, A. W. MEEROW, … & N.

RØNSTED. 2011. Phylogenetic selection of target

species in Amaryllidaceae tribe Haemantheae for

acetylcholinesterase inhibition and aﬃnity to the

serotonin reuptake transport protein. South Afr. J.

Bot. 77: 175-183.

bibliogRaPhy

APG II. 2003. An update of the Angiosperm Phylogeny

Group classiﬁcation for the orders and families of

ﬂowering plants: APG II. Bot. J. Linn. Soc. 141:

https://doi.org/10.1016/j.sajb.2010.07.016

BEAUMONT, M. A. 2010. Approximate Bayesian

computation in evolution and ecology. Ann.

Rev. Ecol. Evol. Syst. 41: 379-406. https://doi.

org/10.1146/annurev-ecolsys-102209-144621

BLANCHARD, J. W. 1990. Narcissus: a guide to wild

daﬀodils. Alpine Garden Society, Surrey.

3

99-436.

https://doi.org/10.1046/j.1095-8339.2003.t01-1-00158.x

APG III. 2009. An update of the Angiosperm Phylogeny

Group classiﬁcation for the orders and families of

ﬂowering plants: APG III. Bot. J. Linn. Soc. 161:

1

05-121.

BLATTNER, F. R. & N. FRIESEN. 2006. Relationship

between Chinese chive (Allium tuberosum) and

its putative progenitor A. ramosum as assessed by

random amplified polymorphic DNA (RAPD).

In: ZEDER, M. A. et al. (eds.), Documenting

domestication: new genetic and archaeological

paradigms, pp. 134-142. California University

Press, Berkeley.

CAMPOS-ROCHA, A., A. DA SILVA MEDEIROS, A.

W. MEEROW, P. ANDRE SANZ-VEGA & J. H.

A. DUTILH. 2022a.A remarkable new species of

Hippeastrum (Amaryllidaceae) from the Serra da

Mantiqueira, Southeastern Brazil. Phytotaxa 571:

197-208. https://doi.org/10.11646/phytotaxa.571.2.6

CAMPOS-ROCHA, A., A. W. MEEROW & D. A.

LIMA. 2019a. The rediscovery of Griﬃnia alba

(Amaryllidaceae), a poorly known and endangered

species. Brittonia 71: 134-143. https://doi.

org/10.1007/s12228-018-9561-1

CAMPOS-ROCHA, A., A. W. MEEROW, E. F. M.

LOPES, J. SEMIR, J. L. S. MAYER & J. H. A.

DUTILH. 2019b. New and reassessed species

of Griﬃnia (Amaryllidaceae) from the Brazilian

Atlantic Forest. Syst. Bot . 44: 310-318.

https://doi.org/10.1600/036364419X15562052252199

CAMPOS-ROCHA, A., A. W. MEEROW, R. M.

MACHADO, J. L. MAYER, ... & J. H. DUTILH.

2022b. Outofthemud:twonewspeciesofHippeastrum

(Amaryllidaceae) from the Doce and Jequitinhonha

River basins, Brazil. Pl. Syst. Evol. 308: 1-25.

https://doi.org/10.1111/j.1095-8339.2009.00996.x

BAEZA, C. & J. MACAYA. 2020. Karyotypic analysis of

Famatina andina (Phil.) Ravenna (Amaryllidaceae):

ﬁrst record of South American Hippeastreae with

secondary centromeric constrictions. Gayana Bot.

7

7: 59-61.

BAEZA, C. M., C. MARIANGEL, E. RUIZ & M.

NEGRITTO. 2009a. El cariotipo fundamental

en Rhodolirium speciosum (Herb.) Ravenna y

R. andicola (Poepp.) Ravenna (Amaryllidaceae).

Gayana Bot. 66: 99-102.

BAEZA, C. M., P. NOVOA, E. RUIZ & M. A.

NEGRITTO. 2009b The fundamental karyotype in

Traubia modesta (Phil.) Ravenna (Amaryllidaceae).

Gayana Bot. 66: 297-300.

BAEZA, C., E. RUIZ, F. ALMENDRAS & P.

PENAILILLO. 2012. Comparative karyotype studies

in species of Miltinea Ravenna, Phycella Lindl. and

Rhodophiala C. Presl (Amaryllidaceae) from Chile.

Rev. Facul. Ciencias Agrarias 44: 193-205.

BAEZA, C. M., N. GARCÍA, F. HERRERA, E. RUIZ

&

M. ROSAS. 2017. Caracterización cromosómica

de Rhodolirium laetum (Phil.) Ravenna

Amaryllidaceae) a través de cariotipiﬁcación e

hibridación in-situ de ADN ribosómico. Gayana Bot.

4: 240-244.

BAKER, W. J., P. BAILEY, V. BARBER,A. BARKER, …

F. FOREST. 2022.Acomprehensive phylogenomic

(

7

&

platform for exploring the Angiosperm Tree of Life.

Syst. Biol . 71: 301-319.

https://doi.org/10.1007/s00606-022-01805-3

https://doi.org/10.1093/sysbio/syab035

BARRETT, S. C. H. & L. D. HARDER. 2005. The

evolution of polymorphic sexual systems in daﬀodils

CAMPOS-ROCHA, A., J. SEMIR, M. PEIXOTO &

J. H. A. DUTILH. 2018. Griﬃnia meerowiana, a

remarkable new species of Amaryllidaceae from

366

A. W. Meerow - Classiﬁcation and phylogeny of Amaryllidaceae

Espírito Santo state, Brazil. Phytotaxa 344: 228-238.

https://doi.org/10.11646/phytotaxa.344.3.3

CHASE, M. W., M. R. DUVALL, H. G. HILLS, J.

G. CONRAN, … & S. HOOT. 1995a. Molecular

phylogenetics of Lilianae. In: RUDALL, P. J. et al.

plastome of the South African species, Amaryllis

belladonna L. (Amaryllidaceae). Mitochondrial DNA

Part B 6: 3393-3395.

https://doi.org/10.1080/23802359.2021.1997121

DUBOUZET, J. G. & K. SHINODA. 1998. Phylogeny of

Allium L. subgenus Melanocrommyum (Webb et Berth.)

Rouy based on DNA sequence analysis of the internal

transcribed spacer region of nrDNA. Theor. Appl. Genet.

97: 541-549. https://doi.org/10.1007/s001220050929

DUBOUZET, J. G., K. SHINODA & N. MURATA.

1997. Phylogeny of Allium L. subgenus Rhizirideum

(G. Don ex Koch) Wendelbo according to dot blot

hybridization with randomly ampliﬁed DNA probes.

Theor. Appl. Genet. 95: 1223-1228.

(eds.), Monocotyledons: systematics and evolution,

vol. 1, pp. 109-137. Royal Botanic Gardens, Kew.

CHASE, M. W., M. F. FAY, D. S. DEVEY, O. MAURIN,

…

& H. S. RAI. 2006. Multi-gene analyses of

monocot relationships: a summary. In: COLUMBUS,

J. T. et al. (eds.), Monocots: comparative biology

and evolution (vol. 1, excluding Poales), pp. 63-75.

Rancho Santa Ana Botanic Garden, Claremont.

CHASE, M. W., J. L. REVEAL & M. F. FAY. 2009.

A subfamilial classification for the expanded

asparagalean families Amaryllidaceae, Asparagaceae

and Xanthorrhoeaceae. Bot. J. Linn. Soc. 161: 132-136.

https://doi.org/10.1111/j.1095-8339.2009.00999.x

https://doi.org/10.1007/s001220050685

DYER, R. A. 1939 (published 1940). Description,

classiﬁcation and phylogeny. A review of the genus

Cyrtanthus. Herbertia 6: 65-103.

CHASE, M. W., D. W. STEVENSON, P. WILKIN &

P. J. RUDALL. 1995b. Monocot systematics: a

combined analysis. In: RUDALL, P. J. et al. (eds.),

Monocotyledons: systematics and evolution, vol. 1, pp.

ESCOBAR, I., E. RUIZ-PONCE, P. J. RUDALL, M.

F. FAY, … & C. M. BAEZA.2020. Phylogenetic

relationships based on nuclear and plastid DNA

sequences reveal recent diversiﬁcation and discordant

patterns of morphological evolution of the Chilean

genera of Gilliesieae (Amaryllidaceae: Allioideae).

Bot. J. Linn. Soc. 97: 541-549.

685-730. Royal Botanic Gardens, Kew.

CHENG, R.-Y., D.-F. XIE, X.-Y. ZHANG, X. FU, ... &

S.-D. ZHOU. 2022. Comparative plastome analysis

of three Amaryllidaceae subfamilies: insights into

variation of genome characteristics, phylogeny, and

adaptive evolution. BioMed Res. Int. 3909596: 1-20.

https://doi.org/10.1155/2022/3909596

COSTA, L., H. JIMENEZ, R. CARVALHO, J.

CARVALHO-SOBRINHO, ... & G. SOUZA. 2020.

Divide to conquer: evolutionary history of Allioideae

tribes (Amaryllidaceae) is linked to distinct trends of

karyotype evolution. Front. Pl. Sci. 11: 320.

https://doi.org/10.1007/s001220050929

FAY, M. F. & M. W. CHASE. 1996. Resurrection

of Themidaceae for the Brodiaea alliance, and

recircumscription of Alliaceae, Amaryllidaceae and

Agapanthoideae. Taxon 45: 441-451.

https://doi.org/10.2307/1224136

FAY, M. F., P. J. RUDALL & M. W. CHASE. 2006.

Molecular studies of subfamily Gilliesioiodeae

(Alliaceae). In: COLUMBUS, J. T. et al. (eds.),

Monocots: comparative biology and evolution (vol.

1, excluding Poales), pp. 365-375. Rancho Santa Ana

Botanic Garden, Claremont.

https://doi.org/10.3389/fpls.2020.00320

CRONN, R., B. J. KNAUS, A. LISTON, P. J. MAUGHAN,

…

& J. UDALL. 2012. Targeted enrichment strategies

for next-generation plant biology. Am. J. Bot. 99: 291-

11. https://doi.org/10.3732/ajb.1100356

DAHLGREN, R. M. T., H. T. CLIFFORD & P. F. YEO.

985. The families of the monocotyledons: structure,

https://doi.org/10.5642/aliso.20062201.30

3

FAY, M. F., P. J. RUDALL, S. SULLIVAN, K. L.

STOBART, … & M. W. CHASE. 2000. Phylogenetic

studies of Asparagales based on four plastid DNA

loci. In: WILSON, K. L. & D. A. MORRISON (eds.),

Monocots-systematics and evolution, vol. 1, pp. 360-

371. CSIRO Publishing, Collingswood.

FELSENSTEIN, J. 2004. Inferring phylogenies. Sinaeuer

Associates, Sutherland.

FERNANDES, A. 1967. Contribution à la connaissance

de la biosystématique de quelques espèces du genre

Narcissus L. Portugaliae Acta Biol., ser. B. Sistem.,

Ecol., Biog. Paleontol. 9: 1-44.

1

evolution and taxonomy. Springer, Berlin.

DAVIS, A. P. 1999. The genus Galanthus: a botanical

magazine monograph. Timber Press Portland, Oregon.

DAVIS, A. P. 2001. The genus Galanthus - snowdrops in

the wild. In: BISHOP, M. et al. (eds.), A monograph

of cultivated Galanthus. pp. 9-63. Griffin Press,

Cheltenham.

DENNEHY, Z., J. BILSBORROW, A. CULHAM, J.

DAVID & K. KÖNYVES. 2021. The complete

367

Bol. Soc. Argent. Bot. 58 (3) 2023

FERNANDES, A. 1968a. Keys to the identiﬁcation of

native and naturalizaed taxa of the genus Narcissus

L. Daﬀodil Tulip Year Book 1968: 37-66.

FERNANDES, A. 1968b. Improvements in the

classiﬁcation of the genus Narcissus L. Pl. Life 24:

GAGE, E., P. WILKIN, M. W. CHASE & J. HAWKINS.

2011. Phylogenetic systematics of Sternbergia

(Amaryllidaceae) based on plastid and ITS sequence

data. Bot. J. Linn. Soc. 166: 149-162.

https://doi.org/10.1111/j.1095-8339.2011.01138.x

GARCÍA, N., C. CUEVAS, J. E. SEPÚLVEDA, A.

CÁDIZ-VÉLIZ & M. J. ROMÁN. 2022a. Two new

species of Miersia and their phylogenetic placements

alongside the recently described M. putaendensis

(Gilliesieae, Allioideae, Amaryllidaceae). PhytoKeys

211: 107-124.

https://doi.org/10.3897/phytokeys.211.87842

GARCÍA, N., R. A. FOLK., A. W. MEEROW, S.

CHAMALA, …. & P. S. SOLTIS. 2017. Deep

reticulation and incomplete lineage sorting

obscure the diploid phylogeny of rain-lilies and

allies (Amaryllidaceae tribe Hippeastreae). Mol.

Phylogenet. Evol . 111: 231-247.

https://doi.org/10.1016/j.ympev.2017.04.003

GARCÍA, N., A. W. MEEROW, S. ARROYO-

LEUENBERGER, R. S. OLIVEIRA, … & W.

S. JUDD. 2019. Generic classification of

Amaryllidaceae tribe Hippeastreae. Taxon 68: 481-

498. https://doi.org/10.1002/tax.12062

5

1-57.

FERNANDES A. 1975. L’évolution chez le genre

Narcissus L. Anales Inst. Bot. A. J. Cavanilles 32:

8

43-872.

FRIESEN, N. 2022. Introduction to edible alliums:

evolution, classification and domestication. In:

RABINOWITCH, H. & B. THOMAS (eds.), Edible

alliums:botany,productionanduses,pp.1-19.CABI,

GB. https://doi.org/10.1079/9781789249996.0001

FRIESEN, N., R. M. FRITSCH, S. POLLNER & F. R.

BLATTNER. 2000. Molecular and morphological

evidence for an origin of the aberrant genus Milula

within Himalayan species of Allium (Alliaceae).

Mol. Phylogenet. Evol. 17: 209-218.

https://doi.org/10.1006/mpev.2000.0844

FRIESEN, N., R. M. FRITSCH & F. R. BLATTNER.

2

006. Phylogeny and new intrageneric classiﬁcation

of Allium (Alliaceae) based on nuclear ribosomal

DNA ITS sequences. In: COLUMBUS, J. T. et

al. (eds.), Monocots: comparative biology and

evolution (vol. 1, excluding Poales), pp. 372-395.

Rancho Santa Ana Botanic Garden, Claremont.

GARCÍA, N. & A. W. MEEROW. 2020. Corrigendum

to: GARCÍA, N., A. W. MEEROW, S. ARROYO-

LEUENBERGER, R. S. OLIVEIRA, … & W.

S. JUDD. 2019. Generic classification of

Amaryllidaceae tribe Hippeastreae [in Taxon 68:

481-498]. Taxon 69: 208-209.

FRIESEN, N. & M. KLAAS. 1998. Origin of some minor

vegetatively propagated Allium crops studied with

RAPD and GISH. Genet. Res. Crop Evol. 45: 511-

5

23.https://doi.org/10.1023/A:1008647700251

https://doi.org/10.1002/tax.12208

FRIESEN, N., S. POLLNER, K. BACHMANN & F.

R. BLATTNER. 1999. RAPDs and noncoding

chloroplast DNA reveal a single origin of the

cultivated Allium fistulosum from A. altaicum

GARCÍA, N., A. W. MEEROW, D. E. SOLTIS & P. S.

SOLTIS. 2014. Testing deep reticulate evolution in

Amaryllidaceae tribe Hippeastreae (Asparagales)

with ITS and chloroplast sequence data. Syst. Bot. 39:

75-89. https://doi.org/10.1600/036364414X678099

GARCÍA N., A. B. SASSONE, R. PINTO & M.

J. ROMÁN. 2022b. Atacamallium minutiflorum

(Amaryllidaceae, Allioideae), new genus and species

from the coastal desert of northern Chile. Taxon 71:

552–562. https://doi.org/10.1002/tax.12684

(Alliaceae). Am. J. Bot. 86: 554-562.

https://doi.org/10.2307/2656817

FRITSCH, R. M. 2001. Taxonomy of the genus Allium:

contribution from IPK Gatersleben. Herbertia 56:

1

9-50.

FRITSCH, R. M., F. R. BLATTNER

&

M.

GURUSHIDZE. 2010. New classiﬁcation of Allium

L. subg. Melanocrommyum (Webb & Berthel) Rouy

GOODMAN, C. S. & B. C. COUGHLIN, B. C. 2000.

Special feature: The evolution of evo-devo biology.

Proc. Nat. Acad. Sci. USA 97: 4424-4456.

(Alliaceae) based on molecular and morphological

characters. Phyton 49: 145-220.

https://doi.org/10.1073/pnas.97.9.4424

FRITSCH, R. M. & N. FRIESEN. 2002. Evolution,

domestication, and taxonomy. In: RABINOWITCH,

H. D. & L. CURRAH (eds.), Allium crop science:

recent advances, pp. 5-30. CABI Publishing,

Wallingford.

GRAHAM, S. W. & S. C. H. BARRETT. 2004.

Phylogenetic reconstruction of the evolution of stylar

polymorphisms in Narcissus (Amaryllidaceae). Am.

J. Bot. 91: 1007-1021.

https://doi.org/10.3732/ajb.91.7.1007

368

A. W. Meerow - Classiﬁcation and phylogeny of Amaryllidaceae

GRAHAM, S.W., J. M. ZGURSKI, M.A. MCPHERSON,

ISING, G. 1970. Evolution of karyotypes in Cyrtanthus.

Hereditas 65: 1-28.

D, M. CHERNIAWSKY, … & H. S. RAI. 2006.

Robust inference of monocot deep phylogeny

using an expanded multigene plastid data set.

In: COLUMBUS, J. T. et al. (eds.), Monocots:

comparative biology and evolution (vol. 1, excluding

Poales), pp. 3-21. Rancho Santa Ana Botanic

Garden, Claremont.

https://doi.org/10.1111/j.1601-5223.1970.tb02305.x

ITO, M., A. KAWAMOTO, Y. KITA, T. YUKAWA &

S. KURITA. 1999. Phylogenetic relationships of

Amaryllidaceae based on matK sequence data. J.

Plant Res. 112: 207-216.

https://doi.org/10.1007/PL00013874

GURUSHIDZE, M., R. M. FRITSCH & F. R.

BLATTNER. 2008. Phylogenetic analysis of Allium

subgen. Melanocrommyum infers cryptic species

and demands a new sectional classiﬁcation. Mol.

Phylogenet. Evol. 49: 997-1007.

JANSSEN, T. & K. BREMER. 2004. The age of major

monocot groups inferred from 800+ rbcL sequences.

Bot. J. Linn. Soc . 146: 385-398.

https://doi.org/10.1111/j.1095-8339.2004.00345.x

JIMENEZ, H. J., A. D. F. DA SILVA, L. S. S. MARTINS,

R. DE CARVALHO & R. M. DE MORAES FILHO.

2020. Comparative genomics plastomes of the

Amaryllidaceae family species. Scientia Plena 16:

060202.

https://doi.org/10.14808/sci.plena.2020.060202

JUDD, W. S., C. S. CAMPBELL, E. A. KELLOGG,

P. F. STEVENS & D M. J. DONOGHUE. 2015.

Plant systematics: a phylogenetic approach, 4th ed.

Sinauer Associates, Sutherland.

https://doi.org/10.1016/j.ympev.2008.09.003

GURUSHIDZE,M.,R.M.FRITSCH&F.R.BLATTNER.

2

010. Species level phylogeny of Allium subgenus

Melanocrommyum-incomplete lineage sorting,

hybridization and trnF gene duplication. Taxon 59:

8

29-840. https://doi.org/10.1002/tax.593012

GURUSHIDZE, M., S. MASHAYEKHI, F. R.

BLATTNER, N. FRIESEN & R. M. FRITSCH.

2

007. Phylogenetic relationships of wild and

cultivated species of Allium section Cepa inferred

by nuclear rDNA ITS sequence analysis. Plant Syst.

Evol. 269: 259-269.

KITCHING, I. J., P. FOREY, C. HUMPHRIES & D.

WILLIAMS. 1998. Cladistics: the theory and

practice of parsimony analysis (No. 11). Oxford

University Press, Oxford.

https://doi.org/10.1007/s00606-007-0596-0

HE, M., C. QU, O. GAO, X. HU & X. HONG.

KÖNYVES, K., J. DAVID & A. CULHAM. 2019.

Jumping through the hoops: the challenges of daﬀodil

(Narcissus ) classiﬁcation. Bot. J. Linn. Soc. 190: 389-

404. https://doi.org/10.1093/botlinnean/boz032

KOSHIMIZU, T. 1930. Carpobiological studies of Crinum

asiaticum L. var. japonicum Bak. Mem. Coll. Sci.,

Kyoto Imp. Univ., Ser. B., Biology 5: 183-227.

KWEMBEYA, E. G., C. S. BJORÅ, B. STEDJE & I.

NORDAL. 2007. Phylogenetic relationships in the

genus Crinum (Amaryllidaceae) with emphasis on

tropical African species: evidence from trnL-F and

nuclear ITS DNA sequence data. Taxon 56: 801-810.

https://doi.org/10.2307/25065862

LARA RICO, R. F., R. VÁSQUEZ CHÁVEZ & M.

A. BURGOS. 2021. The genus Hippeastrum

(Amaryllidaceae) in Bolivia. Paciﬁc Bulb Society,

Leonia.

LARSEN, M. M., A. ADSERSEN, A. P. DAVIS, M.

D. LLEDÓ, ... & N. RØNSTED. 2010. Using a

phylogenetic approach to selection of target plants

in drug discovery of acetylcholinesterase inhibiting

alkaloids in Amaryllidaceae tribe Galantheae.

Biochem. Syst. Ecol . 38: 1026-1034.

2

015. Biological and pharmacological activities

of amaryllidaceae alkaloids. RSC Adv. 5: 16562.

https://doi.org/10.1039/C4RA14666B

HE, X. J., S. GE, J. M. XU & D. Y. HONG. 2000.

Phylogeny of Chinese Allium (Liliaceae) using

PCR-RFLP analysis. Science in China (series C)

4

3:454-463.

HENNIG, W. 1966. Phylogentic systematics. University

of Illinois Press, Urbana.

HERDEN, T., P. HANELT & N. FRIESEN. 2016.

Phylogeny of Allium L. subgenus Anguinum (G.

Don. ex W.D.J. Koch) N. Friesen (Amaryllidaceae).

Mol. Phylogenet. Evol. 95:79-93.

https://doi.org/10.1016/j.ympev.2015.11.004

HIRSCHEGGER, P., J. JAKŠE, P. TRONTELJ & B.

BOHANEC. 2010. Origins of Allium ampeloprasum

horticultural groups and a molecular phylogeny

of the section Allium (Allium: Alliaceae). Mol.

Phylogenet. Evol . 54:488-497.

https://doi.org/10.1016/j.ympev.2009.08.030

HUELSENBECK, J. P. & K. A. CRANDALL. 1997.

Phylogeny estimation and hypothesis testing using

maximum likelihood. Ann. Rev. Ecol. Syst. 28: 437-466.

https://doi.org/10.1016/j.bse.2010.10.005

369

Bol. Soc. Argent. Bot. 58 (3) 2023

LEMMON, A. R., S. A. EMME & E. M. LEMMON.

Narcissus (Amaryllidaceae) challenges current

classiﬁcations and reveals multiple hybridization

events. Taxon 66: 832-854.

2

012. Anchored hybrid enrichment for massively

high-throughput phylogenomics. Syst. Biol. 61: 727-

44. http://doi.org/ 10.1093/sysbio/sys049.

7

https://doi.org/10.12705/664.3

LEMMON, E. M. & A. R. LEMMON. 2013. High-

throughput genomic data in systematics and

phylogenetics. Ann. Rev. Ecol. Evol. Syst. 44:

MATHEW, B. 1983. A review of the genus Sternbergia.

The Plantsman 5: 1-16.

MATHEW, B. 2002. Classification of the genus

Narcissus. In: HANKS, G. R. (ed.), Narcissus and

daﬀodil, pp. 30-52. Taylor and Francis, London.

MEEROW, A. W. 2009. Tilting at windmills: 20 years

of Hippeastrum breeding. Israel J. Pl. Sci. 57:

303-313. http://doi.org/10.1560/IJPS.57.4.303

MEEROW, A. W. 2010. Convergence or reticulation?

Mosaic evolution in the canalized American

Amaryllidaceae. In: SEBERG, O. et al. (eds.),

Diversity, phylogeny and evolution in the

monocotyledons, pp. 145-168. Aarhus University

Press, Aarhus.

MEEROW, A. W. & J. R. CLAYTON. 2004.

Generic relationships among the baccate-fruited

Amaryllidaceae (tribe Haemantheae) inferred

from plastid and nuclear non-coding DNA

sequences. Plant Syst. Evol. 244: 141-155.

9

9-121. https://doi.org/10.1146/annurev-

ecolsys-110512-135822

LI, M. J., J. B.TAN, D. F. XIE, D. Q. HUANG, … & X. J. HE.

2016a. Revisiting the evolutionary events in Allium

subgenus Cyathophora (Amaryllidaceae): insights

into the eﬀect of the Hengduan Mountains Region

(HMR) uplift and quaternary climatic ﬂuctuations

to the environmental changes in the Qinghai-Tibet

Plateau. Mol. Phylogenet. Evol . 94: 802-813.

https://doi.org/10.1016/j.ympev.2015.10.002

LI, Q.-Q., S.-D. ZHOU, X.-J. HE, Y. YU, ... & X.-

Q. WEI. 2010. Phylogeny and biogeography of

Allium (Amaryllidaceae: Allieae) based on nuclear

ribosomal internal transcribed spacer and chloroplast

rps16 sequences, focusing on the inclusion of

species endemic to China. Ann. Bot. 106: 709-733.

https://doi.org/10.1093/aob/mcq177

https://doi.org/10.1007/s00606-003-0085-z

LI, Q.-Q., S. D. ZHOU, D. Q. HUANG, X. J. HE & X. Q.

WEI. 2016b. Molecular phylogeny, divergence time

estimates and historical biogeography within one of

the world’s largest monocot genera. AoB Plants 8:

plw041. https://doi.org/10.1093/aobpla/plw041.

LLEDÓ, M. D., A. P. DAVIS, M. B. CRESPO, M. W.

CHASE & M. F. FAY. 2004. Phylogenetic analysis

of Leucojum and Galanthus (Amaryllidaceae) based

on plastid matK and nuclear ribosomal spacer (ITS)

DNA sequences and morphology. Plant Syst. Evol.

MEEROW, A. W., M. FAY, M. W. CHASE, C. L.

GUY, … & S.-L. YANG. 2000. Phylogeny of

the Amaryllidaceae: molecules and morphology.

In: WILSON, K. L. & D. A. MORRISON (eds.),

Monocots: systematics and evolution, pp. 368-

382. CSIRO Publishing, Collingwood.

MEEROW, A. W., M. F. FAY, C. L. GUY, Q.-B.

LI, … & M. W. CHASE. 1999. Systematics of

Amaryllidaceae based on cladistic analysis of

plastid rbcL and trnL-F sequence data. Am. J. Bot.

86: 1325-1345. https://doi.org/10.2307/2656780

MEEROW, A. W., J. FRANCISCO-ORTEGA, D. N.

KUHN & R. J. SCHNELL. 2006. Phylogenetic

relationships and biogeography within the

Eurasian clade of Amaryllidaceae based on plastid

ndhF and nrDNA ITS sequences: lineage sorting

in a reticulate area? Syst. Bot. 31: 42-60.

2

46: 223-243.

https://doi.org/10.1007/s00606-004-0152-0

LOU, Y.-L., D.-K. MA, Z.-T. JIN, H. WANG, ... & B.-

B. LIU. 2022. Phylogenomic and morphological

evidence reveal a new species of spider lily, Lycoris

longifolia (Amaryllidaceae) from China. Phytokeys

2

10: 79-92.

https://doi.org/10.3897/phytokeys.210.90391

MARQUES, I. C. 2010. Evolutionary outcomes of

natural hybridization in Narcissus (Amaryllidaceae):

the case of N. × perezlarae s.l. Doctoral dissertation.

University of Lisbon, Portugal.

MARQUES, I., J. FUERTES AGUILAR, M. A.

MARTINS-LOUÇAO, F. MOHARREK & H.

N. FELINER. 2017. A three‐genome five‐gene

comprehensive phylogeny of the bulbous genus

https://doi.org/10.1600/036364406775971787

MEEROW, A.W., E. M. GARDNER & K. NAKAMURA.

2020. Phylogenomics of theAndean tetraploid clade of the

American Amaryllidaceae (subfamily Amaryllidoideae):

Unlocking a polyploid generic radiation abetted by

continental geodynamics. Front. Plant Sci. 11: 582422.

https://doi.org/10.3389/fpls.2020.582422

MEEROW,A. W., E. M. GARDNER & K. NAKAMURA.

2023. Corrigendum: Phylogenomics of the Andean

370

A. W. Meerow - Classiﬁcation and phylogeny of Amaryllidaceae

tetraploid clade of the American Amaryllidaceae

subfamily Amaryllidoideae): Unlocking a

polyploid generic radiation abetted by continental

geodynamics. Front. Plant Sci. 14.

MES, T. H. M., R. M. FRITSCH, S. POLLNER & K.

BACHMANN. 1999. Evolution of the chloroplast

genome and polymorphic ITS regions in Allium

subgenus Melanocrommyum . Genome 42: 237-247.

https://doi.org/10.1139/g98-123

(

https://doi.org/10.3389/fpls.2023.1151864

MEEROW,A.W.,C.L.GUY,Q.-B.LI&J.R.CLAYTON.

MÜLLER-DOBLIES, D. & U. MÜLLER-DOBLIES.

1978a. Zum Bauplan von Ungernia, der

einzigen endemischen Amaryllidaceen - Gattung

Zentralasiens. Bot. Jahrb. 99: 249-263.

MÜLLER-DOBLIES, D. & U. MÜLLER-DOBLIES.

1978b. Studies on tribal systematics of

Amaryllidoideae 1. The systematic position of

Lapiedra Lag. Lagascalia 8: 13-23.

NGUYEN, N. H., H. E. DRISCOLL & C. D. SPECHT.

2008. A molecular phylogeny of the wild onions

(Allium;Alliaceae) with a focus on the western North

American center of diversity. Mol. Phylogenet. Evol.

47: 1157-1172.

https://doi.org/10.1016/j.ympev.2007.12.006

OLIVEIRA, R. 2012. O gênero Hippeastrum Herb.

(Amaryllidaceae) no Brasil: evidência de evolução

reticulada e análise de caracteres ﬂorais. PhD Thesis.

Universidade Estadual de Campinas, Brazil.

OLIVEIRA, R. S., J. SEMIR & J. H. A. DUTILH.

2013. Four new endemic species of Hippeastrum

(Amaryllidaceae) from Serra da Canastra, Minas

Gerais State, Brazil. Phytotaxa 145: 38-46.

2

002. Phylogeny of the tribe Hymenocallideae

Amaryllidaceae) based on morphology and

molecular characters. Ann. Missouri Bot. Gard. 89:

00-413. https://doi.org/10.2307/3298600

MEEROW, A. W., C. L. GUY, Q.-B. LI & S.-Y. YANG.

000. Phylogeny of the American Amaryllidaceae

based on nrDNA ITS sequences. Syst. Bot. 25: 708-

26. https://doi.org/10.2307/2666729

MEEROW, A. W., D. J. LEHMILLER & J. R. CLAYTON.

003. Phylogeny and biogeography of Crinum L.

Amaryllidaceae) inferred from nuclear and limited

plastid non-coding DNA sequences. Bot. J. Linn. Soc.

41: 349-363.

(

4

2

7

2

(

1

https://doi.org/10.1046/j.1095-8339.2003.00142.x

MEEROW, A. W., J. L. REVEAL, D. A. SNIJMAN &

J. H. DUTILH. 2007. (1793) Proposal to conserve

the name Amaryllidaceae against Alliaceae, a

“

1

superconservation” proposal. Taxon 56: 1299-

300.

MEEROW, A. W. & D. A. SNIJMAN. 1998.

Amaryllidaceae. In: KUBITZKI, K. (ed.), The

families and genera of vascular plants III.

Flowering plants, monocotyledons: Lilianae

https://doi.org/10.11646/phytotaxa.145.1.4

OLIVEIRA, R. S., J. D. URDAMPILLETA & J. H.

DUTILH.2017.AnewHippeastrum(Amaryllidaceae)

species from Brazil. Phytotaxa 307: 147-152.

https://doi.org/10.11646/phytotaxa.307.2.6

PELLICER, J., O. HIDALGO, J. WALKER, M. W.

CHASE, … & M. F. FAY. 2017. Genome size

dynamics in tribe Gilliesieae (Amaryllidaceae,

subfamilyAllioideae)inthecontextofpolyploidyand

unusual incidence of Robertsonian translocations.

Bot. J. Linn. Soc . 184: 16-31.

(

except Orchidaceae), pp. 83-110. Springer, Berlin.

MEEROW, A. W. & D. A. SNIJMAN. 2001. Phylogeny

of Amaryllidaceae tribe Amaryllideae based on

nrDNA ITS sequences and morphology. Am. J. Bot.

8

8: 2321-2330. https://doi.org/10.2307/3558392

MEEROW, A. W. & D. A. SNIJMAN. 2006. The never-

ending story: multigene approaches to the phylogeny

of Amaryllidaceae, and assessing its familial limits.

In: COLUMBUS, J. T. et al. (eds.), Monocots:

comparative biology and evolution, vol. 1, pp. 365-

https://doi.org/10.1093/botlinnean/box016

3

75. Rancho Santa Ana Botanic Garden, Claremont.

PÉREZ-BARRALES, R., P. VARGAS & J. ARROYO.

2003. Convergent evolution of ﬂower polymorphism

in Narcissus L. (Amaryllidaceae). New Phytol. 161:

235-252.

https://doi.org/10.1046/j.1469-8137.2003.00955.x

PIGG, K. B., F. A. BRYAN & M. L. DEVORE. 2018.

Paleoallium billgenseli gen. et sp. nov.: Fossil

Monocot Remains from the Latest Early Eocene

Republic Flora, Northeastern Washington State,

USA. Int. J. Plant Sci. 179: 477-486.

https://doi.org/10.5642/aliso.20062201.29

MEEROW, A. W., J. VAN SCHEEPEN & J. H. A.

DUTILH. 1997. Transfers from Amaryllis to

Hippeastrum. (Amaryllidaceae). Taxon 46: 15-19.

https://doi.org/10.2307/1224287

MES, T. H. M., N. FRIESEN, R. M. FRITSCH, M.

KLAAS & K. BACHMANN. 1997. Criteria for

sampling in Allium based on chloroplast DNA PCR-

RFLPs. Syst. Bot. 22: 701-712.

https://doi.org/10.2307/2419436

https://doi.org/10.1086/697898

371

Bol. Soc. Argent. Bot. 58 (3) 2023

QIN, W. H., W. Q. MENG, D. ZHANG, Y. WANG, …

SADASIVAIAH, B. K. & S. KARUPPUSAMY. 2018.

Two new species of Pancratium (Amaryllidaceae)

from India. Species 19: 132-139.

SASIKALA, K. & M. KUMARI. 2013. Pancratium

nairii (Amaryllidaceae)-a new species from Kerala,

India. Indian J. For. 36: 543-544.

SARKER, D. DE, M. A. T. JOHNSON, A. REYNOLDS

& P. E. BRANDHAM. 1997. Cytology of the highly

polyploid disjunct species, Allium dregeanum

(Alliaceae), and of some Eurasian relatives. Bot. J.

Linn. Soc . 124: 361-373.

&

K. LIU. 2021. A new Amaryllidaceae genus,

Shoubiaonia, from Yunnan Province, China. Nord. J.

Bot. 39: e02703. https://doi.org/10.1111/njb.02703

RAHN, K. 1998.Alliaceae,Themidaceae. In: KUBITZKI,

K. (ed.), The families and genera of vascular plants

III. Flowering plants, monocotyledons: Lilianae

(except Orchidaceae), pp. 70-78. Springer, Berlin.

RAVEN, P. H. & D. I. AXELROD. 1974. Angiosperm

biogeography and past continental movements. Ann.

Missouri Bot. Gard. 61: 539-673.

https://doi.org/10.2307/2395021

https://doi.org/10.1111/j.1095-8339.1997.tb02002.x

SASSONE, A. B. & S. C. ARROYO-LEUENBERGER.

2018. Revisión taxonómica de las especies del

género sudamericano Tristagma (Amaryllidaceae,

Allioideae). Ann. Missouri Bot. Gard. 103: 163-

174. https://doi.org/10.3417/2018069

SASSONE, A. B., F. R. BLATTNER, L. M. GIUSSANI

& D. H. HOJSGAARD. 2022. First glimpse on

spring starﬂower domestication. Genes 13: 243.

https://doi.org/10.1111/mec.16009

REID, C. & R. A. DYER. 1984. A Review of the southern

African species of Cyrtanthus. American Plant Life

Society, La Jolla.

RENDLE, A. B. 1901. The bulbiform seeds of certain

Amaryllidaceae. J. Roy. Hort. Soc. 26: 89-96.

RØNSTED, N., D. ZUBOV, S. BRUUN-LUND & A.

P. DAVIS. 2013. Snowdrops falling slowly into

place: An improved phylogeny for Galanthus

(Amaryllidaceae). Mol. Phylogenet. Evol. 69: 205-

2

17.

SASSONE, A. B. & L. M. GIUSSANI. 2018.

Reconstructing the phylogenetic history of the

tribe Leucocoryneae (Allioideae): Reticulate

evolution and diversiﬁcation in South America.

Mol. Phylogenet. Evol . 127: 437-448.

https://doi.org/10.1016/j.ympev.2018.04.034

SASSONE, A. B., L. M. GIUSSANI & E. R.

GUAGLIANONE. 2013. Multivariate studies of

Ipheion (Amaryllidaceae, Allioideae) and related

genera. Plant Syst. Evol. 299: 1561-1575.

https://doi.org/10.1007/s00606-013-0819-5

SASSONE, A. B., D. H. HOJSGAARD, L. GIUSSANI,

J. BRASSAC & F. R. BLATTNER. 2021. Genomic,

karyological and morphological changes of South

American garlics (Ipheion) provide insights into

mechanisms of speciation in the Pampean region.

Mol. Ecol. 30: 3716-3729.

https://doi.org/10.1016/j.ympev.2013.05.019

ROUX, J., M. ROSIKIEWICZ & M. ROBINSON‐

RECHAVI. 2015. What to compare and how:

comparative transcriptomics for evo‐devo. J. Exp.

Zool. Part B: Mol. & Develop. Evol. 324: 372-382.

https://doi.org/10.1002/jez.b.22618

RUDALL, P. J., R. M. BATEMAN, M. F. FAY & A.

EASTMAN. 2002. Floral anatomy and systematics

of Alliaceae with particular reference to Gilliesia, a

presumed insect mimic with strongly zygomorphic

ﬂowers. Am. J. Bot. 89: 1867-1883.

https://doi.org/10.3732/ajb.89.12.1867

SAIKI, R. K., D. H. GELFAND, S. STOFFEL, S. J.

SCHARF, ... & H. A. ERLICH. 1988. Primer-

directed enzymatic ampliﬁcation of DNA with a

thermostable DNA polymerase. Science 239: 487-

4

91. https://doi.org/10.1126/science.2448875

https://doi.org/10.1111/mec.16009

SAMOYLOV, A., N. FRIESEN, S. POLLNER &

P. HANELT. 1999. Use of chloroplast DNA

polymorphisms for the phylogenetic study of Allium

subgenus Amerallium and subgenus Bromatorrhiza

SASSONE, A. B., A. LÓPEZ, D. H. HOJSGAARD

& L. M. GIUSSANI. 2018. A novel indicator of

karyotype evolution in the tribe Leucocoryneae

(Allioideae, Amaryllidaceae). J. Plant Res. 131:

211-223.

(Alliaceae) II. Fed. Rep. 110: 103-109. https://doi.

org/10.1002/fedr.19991100118

https://doi.org/10.1007/s10265-017-0987-4

SNIJMAN, D. A. & R. H. ARCHER. 2003.

Amaryllidaceae. In: GERMISHUIZEN, G. & N.

L. MEYER (eds.), Plants of southern Africa: an

annotated checklist (Strelitzia 14), pp. 957-967.

National Botanical Institute, Pretoria.

SAMOYLOV, A., M. KLAAS & P. HANELT. 1995. Use

of chloroplast polymorphisms for the phylogenetic

study of subgenera Amerallium and Bromatorrhiza

(genus Allium ). Fed. Rep. 106: 161-167.

https://doi.org/10.1002/fedr.19951060306

372

A. W. Meerow - Classiﬁcation and phylogeny of Amaryllidaceae

SNIJMAN, D. A. & H. P. LINDER. 1996. Phylogenetic

WEBB, D. A. 1980. Narcissus L. In: TUTIN, T. G. et

al. (eds.), Flora Europaea 5, pp. 78-84. Cambridge

University Press, Cambridge.

relationships, seed characters, and dispersal system

evolution in Amaryllideae (Amaryllidaceae). Ann.

Missouri Bot. Gard. 83: 362-386.

WEICHHARDT-KULESSA, K., T. BÖRNER, J.

https://doi.org/10.2307/2399866

SCHMITZ, U. MÜLLER-DOBLIES & D.

SNIJMAN, D. A. & A. W. MEEROW. 2010. Floral

and macroecological evolution within Cyrtanthus

MÜLLER-DOBLIES. 2000. Controversial

taxonomy of Strumariinae (Amaryllidaceae)

investigated by nuclear rDNA (ITS) sequences.

Plant Syst. Evol. 223: 1-13.

(Amaryllidaceae): inferences from combined analyses

of plastid ndhF and nrDNA ITS sequences. S. Afr. J.

Bot. 76: 217-238.

https://doi.org/10.1007/BF00985323

https://doi.org/10.1016/j.sajb.2009.10.010

WEITEMIER, K., S. C. K. STRAUB, R. C. CRONN,

M. FISHBEIN, … & A. LISTON. 2014. Hyb-Seq:

combining target enrichment and genome skimming

for plant phylogenomics. Appl. Plant Sci. 2: 1400042.

http://doi.org/10.3732/apps.1400042.

SNIJMAN, D. A. & G. WILLIAMSON. 1994. A

taxonomic re-assessment of Ammocharis

herrei and Cybistetes longifolia (Amaryllideae:

Amaryllidaceae). Bothalia 24: 127-132.

SNOEIJER, W. 2004. Agapanthus: a revision of the

genus. Timber Press, Portland.

WILDE DUYFJES, B. E. E. DE. 1976. A revision of the

genus Allium L. (Liliaceae) in Africa. H. Veenman and

Zonen B.V., Wageningen.

WILEY, E. O. 1981. Phylogenetics, the theory and practice

of phylogenetic systematics. John Wiley and Sons, New

York.

STAFFORD, G. I., M. J. WIKKELSØ, L. NANCKE,

A. K. JÄGER, ... & N. RØNSTED. 2016. The

first phylogenetic hypothesis for the southern

African endemic genus Tulbaghia (Amaryllidaceae,

Allioideae) based on plastid and nuclear DNA

sequences. Bot. J. Linn. Soc. 181: 156-170.

https://doi.org/10.1111/boj.12417

WILSENACH, R. 1963. A cytotaxonomic study of the

genus Cyrtanthus . Cytologia 28: 170-180.

https://doi.org/10.1508/cytologia.28.170

STERN, F. C. 1956. Snowdrops and snowﬂakes. A study

of the genera Galanthus and Leucojum. The Royal

Horticultural Society, London.

WING, S. L., F. HERRERA, C. A. JARAMILLO, C.

GÓMEZ-NAVARRO, … & C. C. LABANDEIRA,

2009. Late Paleocene fossils from the Cerrejón

Formation, Colombia, are the earliest record of

Neotropicalrainforest.Proc.Nat.Acad.Sci.106:18627-

18632. https://doi.org/10.1073/pnas.0905130106

XIE, D. F., J. B. TAN, Y. YU, L. J. GUI, … & X. J. HE.

2020. Insights into phylogeny, age and evolution of

Allium (Amaryllidaceae) based on the whole plastome

sequences. Ann. Bot. 125: 1039-1055.

STRYDOM, A., R. KLEYNHANS & J. J. SPIES.

2

007. Chromosome studies on African plants. 20.

Karyotypes of some Cyrtanthus species. Bothalia

7: 103-108.

3

TRAUB, H. P. 1963. Genera of the Amaryllidaceae.

American Plant Life Society, La Jolla.

TRAUB, H. P. & H. N. MOLDENKE. 1949.

Amaryllidaceae: tribe Amarylleae. American

Amaryllis Society, Stanford.

VOSA, C. 2007. Prototulbaghia (Alliaceae), a new genus

of the Alliaceae family from the Leolo mountains in

Sekhukhuneland, South Africa. Caryologia 60: 273-

https://doi.org/10.1093/aob/mcaa024

ZHANG, F., N. WANG, G. CHENG, X. SHU, ... & Z.

WANG. 2021. Comparative chloroplast genomes of

four Lycoris species (Amaryllidaceae) provides new

insight into interspeciﬁc relationship and phylogeny.

Biology 10: 715.

278. https://doi.org/10.1080/00087114.2007.10797948

VOSA, C. G. 2009. An updated and illustrated taxonomic

synopsis of the genus Tulbaghia (Alliaceae).

Herbertia 63: 208-219.

WATERS, M. T., A. M. M. TILEY, E. M. KRAMER,

A. W. MEEROW, … & R. W. SCOTLAND. 2013.

The corona of the daﬀodil Narcissus bulbocodium

shares stamen-like identity and is distinct from the

orthodox ﬂoral whorls. Plant J. 74: 615-625.

https://doi.org/10.1111/tpj.12150

https://doi.org/10.3390/biology10080715

ZHANG, S. Y., H. T. WANG, Y. F. HU, W. ZHANG, … &

J. W. SHAO. 2022. Lycoris insularis (Amaryllidaceae),

a new species from eastern China revealed by

morphological and molecular evidence. Phytokeys

206: 153-165.

https://doi.org/10.3897/phytokeys.206.90720

ZÖLLNER, O. & L. ARRIAGADA. 1998. The tribe

Gilliesieae (Alliaceae) in Chile. Herbertia 53: 104-107.

373