Phytotaxa 376 (6): 227–253
http://www.mapress.com/j/pt/
Copyright © 2018 Magnolia Press
ISSN 1179-3155 (print edition)
Article
PHYTOTAXA
ISSN 1179-3163 (online edition)
https://doi.org/10.11646/phytotaxa.376.6.1
Phylogenetic relationships of Hechtia (Hechtioideae; Bromeliaceae)
IVÓN M. RAMÍREZ-MORILLO1,*, GERMÁN CARNEVALI1,5, JUAN P. PINZÓN2, KATYA ROMERO-SOLER1, N.
RAIGOZA1, C. HORNUNG-LEONI3, R. DUNO1, J. L. TAPIA-MUÑOZ1 & I. ECHEVARRÍA4
1
Centro de Investigación Científica de Yucatán, A. C. Unidad de Recursos Naturales. Calle 43 # 130 x 32 y 34. Colonia Chuburná de
Hidalgo. Mérida, Yucatán, CP 97205, Mexico.
2
Departamento de Botánica, Campus de Ciencias Biológicas y Agropecuarias, Universidad Autónoma de Yucatán, Carretera MéridaXmatkuil, Km. 15.5, Apdo. Postal 4-115 Itzimná, CP 97100, Mérida, Yucatán, Mexico.
3
Universidad Autónoma del Estado de Hidalgo, Centro de Investigaciones Biológicas, Instituto de Ciencias Básicas e Ingeniería, Km
4.5 Carretera Pachuca-Tulancingo, Mineral de La Reforma, Hidalgo, CP 42184, Mexico.
4
Centro de Investigación Científica de Yucatán, A. C. Unidad de Bioquímica y Biología Molecular de Plantas. Calle 43 # 130 x 32 y 34.
Colonia Chuburná de Hidalgo. Mérida, Yucatán, CP 97205, Mexico.
5
Orchid Herbarium of Oakes Ames, Harvard University Herbaria, 22 Divinity Avenue, Cambridge, Massachusetts 02138, U.S.A.
*Corresponding author: Email: ramirez@cicy.mx
Abstract
This is the first phylogenetic analysis of the Megamexican Bromeliaceae genus Hechtia and includes 82.6 % of the known
taxa. We used plastid (ycf1, rpl32-trnL intergenic spacer), and nuclear (PRK) DNA regions, as well as morphological characters. We generated 244 new sequences for a total of 62 taxa (including 12 species of the outgroup). Results of combined data
using parsimony and Bayesian inference reveal the monophyly of Hechtia, as well as identify five well supported clades:
(1) a clade (H. tillandsioides complex) as the sister group to the rest of Hechtia; (2) a clade including the species of the H.
guatemalensis complex, distributed in Southern Megamexico; the remaining taxa of the genus are retained in a clade which
consists of three well-supported clades; (3) the H. glomerata complex distributed in the Gulf of Mexico drainage; (4) a clade
of two species (H. deceptrix and H. epigyna) that share an inferior ovary and are distributed north of the Tehuantepec Isthmus in the Sierra Madre Oriental; and (5) an internally poorly resolved clade with the remaining species containing several
well-supported, geographically restricted clades. At this time it is uncertain what part of Megamexico was first invaded by
the ancestor of Hechtia. Regardless, it becomes clear that from the original point of invasion in what is now Megamexico, it
radiated into restricted geographical realms with secondary radiations occurring within them, which resulted in some recurrent particular evolutionary trends most likely associated with the invasion of dry, highly seasonal climates, or cooler areas
subject to occasional frosts. Lateral inflorescences and flower morphology suggesting pollination syndromes other than
melittophily (psychophily/trochilophily) have evolved more than once in Hechtia.
Key words: Character evolution-Endemism-Megamexico
Resumen
Este es el primer análisis filogenético del género Megamexicano Hechtia (Hechtioideae; Bromeliaceae), el cual incluye al
82.6 % de los taxones conocidos. Usamos las regiones de ADN de plástidos (ycf1, rpl32-trnL espaciador intergénico) y nucleares (PRK), así como caracteres morfológicos. Generamos 244 nuevas secuencias para un total de 62 taxones (incluidas
12 especies del grupo externo). Los resultados de datos combinados usando parsimonia e inferencia Bayesiana revelan la
monofilia de Hechtia, así como la identificación de cinco clados bien apoyados: (1) un clado (complejo H. tillandsioides)
como el grupo hermano del resto de Hechtia; (2) un clado que incluye especies del complejo H. guatemalensis; los taxones
restantes del género se agrupan en un clado el cual consta de tres linajes bien respaldados; (3) el complejo H. glomerata
distribuido en la vertiente del Golfo de México; (4) un clado de dos especies (H. deceptrix y H. epigyna) que comparten
un ovario inferior y se distribuyen al norte del Istmo de Tehuantepec en la Sierra Madre Oriental; y (5) un clado interno
pobremente resuelto con las especies restantes que contienen varios clados bien respaldados y restringidos geográficamente.
Actualmente es incierto el punto y la via de entrada del ancestro de Hechtia a Megaméxico, pero es muy probable que una
vez que lo invadió, irradió a reinos geográficos restringidos con radiaciones secundarias dentro de ellos, lo que dio lugar
a algunas tendencias evolutivas particulares recurrentes muy probablemente asociadas con la invasión de climas secos y
altamente estacionales, o áreas más frías sujetas a heladas ocasionales. Las inflorescencias laterales y morfología floral que
Accepted by Eric Gouda: 20 Oct. 2018; published: 22 Nov. 2018
227
sugiere otros síndromes de polinización diferentes a la melitofilia (psicofilia / troquilofilia), han evolucionado más de una
vez en Hechtia.
Palabras clave: Evolución de caracteres-Endemismo-Megaméxico
Introduction
The most recent classifications of Bromeliaceae using combined analysis of eight regions of plastid DNA, recognize
eight lineages, each treated as a subfamily by Givnish et al. (2007, 2011, 2014). Of the three classic subfamilies
recognized by Smith & Downs (1974), only Tillandsioideae and Bromelioideae are retrieved as monophyletic and
nested within a broadly non-monophyletic Pitcairnioideae, a group held together by symplesiomorphies. Pitcairnioideae
was thus recircumscribed as most of its original members now reside in several newly recognized subfamilies
(e.g., Brocchinioideae, Lindmanioideae, Puyoideae, Hechtioideae, and Navioideae, which are related as follows:
(Brocchinioideae, (Lindmanioideae, (Tillandsioideae, (Hechtioideae, (Navioideae, (Pitcairnioideae, (Puyoideae,
Bromelioideae))))))). Givnish et al. (2014) further suggested that the family originated ca. 97.5 Ma in the Guayana
Shield from where they radiated to other Neotropical areas 16–15.2 Ma, including a single long-distance dispersion
event to Western Africa ca. 9.3 Mya.
Previous phylogenetic analysis containing species of Hechtia Klotzsch (1835: 401) (i.e. Horres et al. 2000; Reinert,
Russo & Salles 2003; Crayn, Winter & Smith 2004; Givnish et al. 2004, 2007, 2011) include less that 6 % (3 to 4) of
the currently known species. Nevertheless, Hechtia has always been retrieved as monophyletic in studies at different
taxonomic levels (Horres et al. 2000; Crayn et al. 2004; Givnish et al. 2004, 2007, 2011). Furthermore, Givnish et al.
(2011) proposed that Hechtia arose ca. 16.6 Ma and invaded the current territory of Megamexico, where the ancestors
of most modern species probably differentiated ca. 10.3 Ma. Currently, there is neither a modern systematic revision
of the genus (the last one is that of Smith & Downs, 1974) nor a phylogenetic hypothesis of internal relationships.
Hechtioideae comprises a single genus, Hechtia within which 75 species are currently recognized (Gouda et al.
(cont.updated) and there is still several more awaiting nomenclatural recognition. Within Bromeliaceae, the subfamily
is characterized by several features (sensu Givnish et al. 2007). These include capsular fruits, winged or almost naked
seeds, dioecy, succulent leaves (see Givinsh et al. 2007) spiny or rarely entire foliar margins, and lack of stellate
sclerenchyma. In addition, plants are terrestrial or lithophytic, growing over limestone, gypsum, or volcanic rocks. The
flowers are fragrant (with the exception of flowers with putatively psychophilous or ornithophilous syndromes such as
Hechtia rosea E. Morren ex Baker, H. iltisii Burt-Utley & Utley, and H. meziana L.B. Sm.), the pistillate ones with a
simple-erect stigma and staminodia whereas staminate flowers bear stamens as well as pistillodes.
Hechtia is restricted to and spans most of Megamexico III (Rzedowski 1991), a region encompassing all of
the Chihuahuan and Sonoran deserts at the northern limit (Texas in U.S.A.), and extending southwards to northern
Nicaragua (Nueva Segovia and Jinotega Departments; Figure 1), although most of the species (94 %) are restricted
to Mexico proper (Ramírez and Jiménez 2012; Espejo-Serna 2012). The genus reaches its highest richness in the
biogeographic provinces of Sierra Madre del Sur, Veracruzan, Chiapas Highlands, Pacific Lowlands, Balsas Basin,
Transmexican Volcanic Belt, and Mexican Plateau (circumscribed as in Morrone 2014). About half of the species are
restricted to a single province, whereas 35 % occur in two provinces. An additional 6 % are recorded from three or
more provinces. When more than one, the provinces involved in the distribution of the taxa are always contiguous
(Pech-Cárdenas 2015); suggesting long range dispersal is unlikely. Hechtia taxa occur at a wide range of elevations,
from sea level to 2700 m. They occur in xerophytic shrublands (where they can be conspicuous floristic elements) as
well as in Quercus-Pinus associations, or even in tropical dry forests, where they are less diverse.
Currently, Hechtia is an insufficiently known taxonomic group. Advancement in its understanding has been
hindered by its dioecy coupled with floral dimorphism and phenotypic plasticity. Also, the cumbersome, heavily spined
plants that are often very large (e.g. Hechtia myriantha Mez; Espejo, López-Ferrari & Ramírez-Morillo 2005) have
usually resulted in the accumulation of fragmentary herbarium specimens, difficulting the understanding of species
variation and their boundaries. Many Hechtia species have been described from fruiting specimens because fruits
are long lasting and relatively showy as opposed to the inconspicuous flowers lasting but one day; thus, plants are
commonly collected in fruiting condition. In other, somewhat better cases, the type specimens are staminate; frequently
the flowering period of staminate plants are longer, although individual flowers equally last one day. Additionally, sex
ratios are usually male-skewed in many species, as it has been documented in Hechtia schottii Baker (Ramírez et al.
2008). A taxonomic consequence of the disparity in sexual morph representation in herbaria is that many species are
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RAMÍREZ-MORILLO ET AL.
only partially known and the taxonomist´s task here consists in documenting the species to fill up voids of information.
In many cases, it has been necessary to epitypify species whose types include only one sex, rendering the species
ambiguously diagnosable (Ramírez-Morillo et al. 2012) or publish accounts of species where both sexual morphs
as well as fruits are documented and reconciled (Ramírez, Jiménez & Treviño 2013; Ramírez et al. 2014; RamírezMorillo et al. 2016).
FIGURE 1. Distribution of Hechtia (blue dots) in Megamexico, based on herbarium specimens (sensu Pech-Cárdenas 2015).
Most modern Hechtia taxonomists have taken up the task to fully document morphologically their new species,
as well as providing field observations to understand natural variation (Burt-Utley & Utley 1993; Burt-Utley et al.
2011; Espejo-Serna et al. 2008; Espejo-Serna et al. 2010; García-Ruiz et al. 2014; González-Rocha et al. 2014; LópezFerrari & Espejo-Serna 2013, 2014; Martínez-Correa et al. 2010; Ramírez-Morillo et al. 2014; Ramírez-Morillo et
al. 2015; Ramírez-Morillo et al. 2016). In the course of these studies, we have been able to observe discontinuities
in several relevant characters as well as identify species groups with distinctive biogeographies. There is variation in
growth patterns (Ramírez-Morillo et al. 2014) that range from plants with monopodial architecture to others where
sympodial growth may come along with precociously blooming rosettes (resulting in apparently lateral inflorescences)
or these flowering terminally when rosettes are fully mature; these growth patterns are also associated with altitudinal
and biogeographical distribution patterns as it will be discussed later. There is also variation in vegetative features
such as rosette size, foliar margin and spination or the presence of stolons. Between taxa and clades within the genus,
inflorescences are variable in architecture and flowers are equally variable in indument, as well as texture of sepals
and petals, ovary position, and the morphology of fruits and seeds. Pollen is also variable in size and ornamentation
of exine (Herrera 2016) whereas seed size and its external features are taxonomically informative (Fatzer 1989).
Some anatomical features have been analyzed (Martínez-Correa et al. 2010; Flores 1975) and found potentially useful
in disentangling the relationships within the genus. Several of the morphological groups within Hechtia also share
distinctive, coherent biogeographical ranges (Pech-Cárdenas 2015). All this evidence lends clues to the evolutionary
history of the genus that should reveal itself in phylogenetic analysis.
PHYLOGENETICS OF HECHTIA
Phytotaxa 376 (6) © 2018 Magnolia Press • 229
In this study we explore the monophyly and internal relationships of Hechtia with a taxonomic sampling far
exceeding any previous study. To accomplish this, we use both morphological and molecular data of 82.6 % of the
known species of the genus. We contextualize our sampling with representatives of the seven remaining bromeliad
subfamilies to assess sister-taxa relationships. This study will lie the foundation for forthcoming articles aimed at
further investigation of character evolution and an analysis of the factors driving the radiations of this Megamexico
III-endemic clade.
We aim at addressing the following questions:—is Hechtia a monophyletic assemblage of taxa when tested with
a larger sampling and new evidence?;—what are the internal relationships of the group and what synapomorphies
support clades identified by analysis?;—have lateral inflorescence, inferior ovary, and flower morphology suggesting
the psychophily/trochyphily syndromes evolved one or several times in the genus?
Materials and methods
Taxa selection
This study includes representatives of all subfamilies recognized by Givnish et al. (2007), accounting for a total of 62
taxa, 12 of which constitute an outgroup, and a total of 248 sequences, 244 new, four obtained from the GenBank (see
Appendix 1). The outgroup includes taxa of the seven additional subfamilies: Bromelioideae (2 spp.), Brocchinioideae
(1 sp.), Navioideae (1 sp.), Lindmanioideae (2 spp.), Pitcairnioideae (2 spp.), Puyoideae (1 sp.), and Tillandsioideae
(3 spp.). To address questions regarding the internal relations of Hechtia, we selected 50 species (accounting for ca.
82.6 % of currently recognized taxa in the genus), including four undescribed yet well-characterized species from the
Mexican States of Chiapas (CHIS), Guanajuato (GTO), and Tamaulipas (TAMPS), these are: Hechtia sp. TAMPS:
Salto, TAMPS: Jaumave, GTO: Xichú, and CHIS: Comitán.
Plant material
Samples were taken from live plants that were field collected, obtained in exchange or purchased from trustworthy
sources. Seed of several species were sown and grown at the Jardín Botánico Regional “Roger Orellana” of CICY and
in private greenhouses. Material was obtained in Mexico, the USA, Guatemala, and Honduras. Silica gel-dried samples
were obtained as exchange from the Marie Selby Botanical Gardens, the Rio de Janeiro Botanical Garden (Brazil), and
the DNA bank of the Missouri Botanical Garden. Furthermore, private collectors or growers donated materials used in
this study (see Appendix 1).
DNA extraction, amplification and sequencing
To yield a more robust phylogenetic tree than previous attempts, we chose three plastid DNA regions (rpl32-trnL
intergenic spacer (UAG) (from here onwards referred to as rpl32-trnL), and two fragments of the ycf1 gene. We
also sequenced a fragment of the low-copy, nuclear PRK gene. The rpl32-trnL region of circa 1,018 bp (Shaw et
al. 2007) is found in the short single copy (SSC) region of the plastid DNA and several studies (e.g., Givnish et al.
2011) have demonstrated that it is useful in phylogenetic analysis. The ycf1 (plastid yeast cadmium factor protein 1
or TIC214), of approximately 5,500 bp (one of the longest genes of the plastid genome) is also mostly located in the
SSC region and is the most variable coding plastid region in Angiosperms (Dong et al. 2015) even larger than that of
matK (Neubig et al. 2009). Recently, Castello et al. (2016) and Pinzón et al. (2016) employed this region to resolve
the relationships within the Tillandsia capillaris Ruiz & Pav. complex (Tillandsioideae) and Tillandsia utriculata L.
complex, respectively, whereas Barfuss et al. (2016) successfully used it in a phylogenetic analysis that was the base
for a taxonomic revision of Tillandsioideae. In these cases, larger absolute numbers of informative sites were found
as compared to the plastid regions previously employed. Finally, the low-copy PRK (Phosphoribulokinase) gene has
proven to be highly informative in Bromeliaceae (Schulte, Barfuss & Zizka 2009; Barfuss 2012).
DNA extraction was performed with fresh or silica gel dried tissue. The DNeasy Plant Mini Kit (QIAGEN) was
used following the manufacturer specifications. In a few cases, the Mini-prep 2× CTAB method (Vázquez-Lobo 1996,
modified) was employed. To amplify the rpl32-trnL intergenic spacer the following primers were used: trnL(UAG)
and rpl32-F (Shaw et al. 2007). The ycf1-a fragment was amplified with primers ycf1(part 2) whereas for the ycf1b fragment, the ycf1-4492f-br and ycf1-5440r-br primers were used (Barfuss et al. 2016; Castello et al. 2016). The
nuclear PRK region was amplified with the following primers: prk-735f (Schulte et al. 2009), prk-630f, prk-890r, and
prk-1057r (Barfuss 2012).
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RAMÍREZ-MORILLO ET AL.
The following PCR protocol was employed for a final volume of 25 μl in each reaction: 2.5 μl Buffer 10x
(Invitrogen), 1.85 μl MgCl2 50μM (Invitrogen), 0.4 μl dNTP 10X, 0.5 μl 10x each primer, 0.2 μl Taq DNA polymerase
5 U/μl (Invitrogen), 2 μl DNA, and the volume was completed with dH2O. To amplify the PRK region, 2.5 μl BSA
0.04 % was added to the solution. PCR reactions were conducted in a Veriti® 96-Well Fast Thermal Cycler (Applied
Biosystems, Foster City, CA, USA) under the following conditions: initial denaturation at 95 °C for 2 min, followed
by 40 cycles of 95 °C for 30 s (35 cycles for both ycf1 fragments), annealing at 62.5 °C (rpl32-trnL), 58 °C (both ycf1
fragments) and 62 °C (PRK) for 5 s, a period of 70 °C for 1.3 min, and a final extension at 70 °C for 7 min.
To assess whether PCR reactions were successful, an agarose (1.5 %) gel electrophoresis was performed with
ethidium bromide as a dye. To accomplish this, 5 μl of the PCR product were placed and photographed in an UV
transiluminator. Samples were then sent to MACROGEN (South Korea; http://dna.macrogen.com) for sequencing.
Primers for sequencing were the same as for amplification with the exception of the internal primers prk-735f and prk890r, used for sequencing nuclear PRK.
Morphological characters
Seven morphological characters were assessed and coded from the analysis of field populations, cultivated plants,
material in spirits (70 % EtOH, 5 % glycerin; flowers and fruits), and herbarium specimens. Specimens from the
following herbaria (acronyms according to Thiers, B., 2018) were available for analysis: ASU, B, BIGU, CHAPA,
CICY, EAP, ENCB, F, GH, HGOM, HUH, IBUG, IZTA, K, LAGU, LL, MEXU, MHES, MICH, MO, NY, QMEX,
SEL, TEFH, TEX, UAMIZ, US, W, WU, XAL, and ZEA. All structural characters employed are qualitative and
discrete and are described as follows:
(1) Growth pattern. Three different patterns were identified by Ramírez-Morillo et al. (2014) and were here
codified as follows (see Appendix 2 for codification for each species): [0] SSP-Strict Sympodial Pattern: here, the
apical meristem of a fully grown rosette produces an inflorescence; after fruiting the rosette dies, producing one or more
offsets in a basal position, resulting in cespitose plants and then usually forming colonies consisting of several rosettes.
[1] PMP-Pseudomonopodial Pattern: a rosette produces truly lateral inflorescences and the apical meristem remains
indefinitely active, never making a transition into a floral meristem; thus, rosettes have indefinite vegetative growth,
eventually becoming very large and flowering continuously as long as the rosette is alive. [2] SPFP- Sympodial with
Precocious-Flowering Pattern: the inflorescence emerges from the center of a newly-forming shoot or rosette (thus
precocious) that never fully develops; on occasion, fully developed rosettes flower simultaneously with the precocious
ones.
(2) Foliar margin. This character ranges from entire to serrulate (small teeth oriented to the apex of the leaf), to
denticulate (minute teeth perpendicular to mid nerve) to spiny (spines antrorse and/or retrorse with hard, strong teeth):
[0] Entire, [1] Serrulate, [2] Spiny, [3] Denticulate.
(3) Style. It varies from absent with the stigmatic lobes emerging from the top of the ovary, to slightly developed
or to conspicuous and elongated: [0] Absent, [1] Present.
(4) Ovary position. It varies in Hechtia from completely inferior to completely superior, with intermediate states
where the ovary is half-inferior or ¾ inferior: [0] Inferior, [1] Superior, [2] Partially inferior.
(5) Flower fragrance. Its presence is very rare in Bromeliaceae, but all species of Hechtia (with the exception of
those with red petals (the presumably hummingbird or butterfly-pollinated H. meziana, H. rosea, and H. iltisii) produce
sweetly fragrant flowers (stronger in male flowers): [0] Absent, [1] Present.
(6) Fruits. They vary from capsules with plumose, winged or naked seeds to fleshy fruits (berries), usually with
naked seeds: [0] Capsules, [1] Berries.
(7) Flower sex. Flowers have both sexual organs or they are either staminate or pistillate: [0] Hermaphrodite, [1]
Unisexual.
Sequences assembly, alignment, and coding of insertions/deletions
The sequences generated were assembled with Geneious 7.1.3 (Kearse et al. 2012). Automated alignments of both
our and GenBank sequences for each DNA region were produced with MUSCLE V3.8.31 (Edgar 2004) with the
Mesquite V3.04 (Maddison & Maddison 2015) visual interface; these alignments were manually refined afterwards
with the PhyDe V0.9971 editor (Müller et al. 2010). Indels were coded as binary characters following the simple
coding method of Simmons & Ochoterena (2000), through SeqState V1.4.1 (Müller 2005). Information about taxa and
sequences included in this study are shown on Appendix 1.
PHYLOGENETICS OF HECHTIA
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Phylogenetic analysis
We initially conducted parsimony analyses (MP) of data from available sources of evidence: (1) seven morphological
characters and 62 terminals; (2) each individual plastid DNA region (rpl32-trnL, rpl32-trnL +indels, ycf1-a, and
ycf1-b) with 60–61 terminals; (3) nuclear PRK region with 58 terminals; (4) concatenated plastid regions with 62
terminals; (5) all plastid regions plus morphology; (6) all evidence (plastid and nuclear regions and morphology)
with 62 terminals. Congruence between matrices was evaluated with the use of the Incongruence Length Difference
test (ILD; Farris et al. 1995). This test was conducted in PAUP* V4.0a151 (Swofford 2003) with 1000 iterations per
analysis. Phylogenetic reconstructions with Maximum Parsimony (MP) were performed with 500 iterations of the
Parsimony Ratchet algorithm (Nixon 1999) through TNT v 1.5 (Goloboff, Farris & Nixon 2000). In all cases, Fitch
parsimony (Fitch 1971) was implemented. Support of nodes was estimated with 1000 iterations of the bootstrap (BT)
(Felsenstein 1985). Phylogenetic reconstructions were also performed under a Bayesian Inference (BI) approach for
each the following data set: plastid, nuclear, and all evidence. Bayesian inference analyzes were performed with the
use of MrBayes V3.2.6 (Ronquist & Huelsenbeck 2003) as implemented in the CIPRES Science Gateway platform
(https://www.phylo.org/portal2/login!input.action). Nucleotidic substitution models were assessed with jModelTest
2.1.7 (Darriba et al. 2012) for each DNA partition. Substitution models best fitting the evolution of each nucleotidic
partition were selected following the Akaike Information Criterion (AIC). The GTR + Γ model was identified as best
for the evolution of the rpl32-trnL, ycf1-a, and ycf1-b regions whereas HKY + Γ was selected as the model best fitting
the evolution of the PRK region. For the rpl32-trnL region, indels were treated as ‘restriction’ data, and thus, the
‘variable’ option was implemented.
Two independent runs, each of 20.000.000 generations were performed; each run consisted of a “cold” and three
“hot” chains. Each 1000 generations, a single tree was sampled. 25 % of the initial samples were discarded as burnin before data reached stationarity. Other parameters were set as for the default settings in Mr. Bayes. Convergence
diagnosis was done in Tracer V1.6 (Rambaut et al. 2014) using the Effective Sample Sizes (ESS) values, which were
all > 200. Clade Posterior Probabilities (PP) was assessed by a 50 % majority-rule consensus of trees retained after
burn-in. Resulting tree was visualized and edited in Fig Tree v1.4.2 (http://tree.bio.ed.ac.uk/software/figtree/) and
Mesquite V3.04.
An ancestral state reconstruction analysis was performed through parsimony using MESQUITE 2.75 (Maddison
and Maddison 2015) for the same morphological characters used for the phylogenetic reconstruction (Appendix 2).
Results
Morphological characters and sequence alignments characteristics
Table 1 resumes characteristics of the different sources of evidence employed in the analysis, including DNA regions
(plastid and nuclear) and morphology. For each matrix, we indicated alignment size (pb), constant, variable, and
parsimony-informative sites, number of resulting equally most-parsimonious trees and their length, number of taxa in
each analysis, as well as consistency (CI) and retention (RI) indexes.
DNA regions showed differences in variable and parsimony-informative sites, with the PRK nuclear region
containing the highest number of variable sites and parsimony-informative sites, whereas the region with the lowest
percentage of variable characters was rpl32-trnL and the ycf1-a region displayed the lowest percentage of parsimonyinformative characters. However, if we compare all plastid DNA regions with the nuclear PRK region, the percentage
of variable sites is very dissimilar (16.2 % for plastid DNA, considering rpl32-trnL without indels; 49.3 % for PRK);
it was even more different when considering the number of parsimony-informative characters (plastid DNA 6.8 %,
25.4 % for PRK). Coding of indels of the rpl32-trnL region resulted for this specific region in an increase of the
parsimony-informative sites of only 1.2 %, but produced more trees, these most parsimonious (MPT´s); it also resulted
in a decrease of the consistency and retention indexes. The addition of the seven morphological parsimony informative
characters to the PRK matrix resulted in fewer trees, these shorter with higher CI and RI. Upon addition of the seven
morphological characters to the plastid DNA regions matrix, the values of CI and RI increased, and the number of
MPT´s decreased and shorter trees were found. In the case of the combined analysis, adding morphological data to all
molecular evidence caused an increase on the number of maximally parsimonious trees, these shorter, and with lower
values of CI.
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PHYLOGENETICS OF HECHTIA
Table 1. General statistics of the maximum parsimony phylogenetic reconstruction in Hechtia using DNA regions (plastid, nuclear, and morphology). Characteristics
include alignment length, number and percentage of variable and parsimony-informative sites, taxa included in the analysis, number of MPTs, and their statistics (L,
CI, and RI).
Phytotaxa 376 (6) © 2018 Magnolia Press • 233
Marker
Aligned size (bp)
Constant sites
(number/%)
Variable sites
(number/%)
Parsimony informative
characters (number/%)
# taxa
# trees
Tree length
CI
RI
rpl32-trnL
1165
995/85.4 %
170/14.6 %
68/5.8 %
61
1210
804
0.66
0.81
rpl32-trnL + indels
1179
995/84.4 %
184/15.6 %
82/7 %
61
9428
182
0.52
0.78
ycf1-a
906
760/83.9 %
146/16.1 %
49/5.4 %
60
5430
109
0.54
0.75
ycf1-b
904
749/82.9 %
155/17.1%
72/8 %
60
9236
136
0.58
0.78
PRK
1228
622/50.7 %
606/49.3 %
312/25.4 %
58
4683
797
0.56
0.75
Morphology
7
7/100%
7/100%
7/100%
62
1269
16
0.75
0.96
PRK + morphology
1235
622/50.4%
613/49.6%
319/25.8%
58
3455
778
0.58
0.78
cpDNA
2989
2504/83.8%
485/16.2%
203/6.8%
62
9392
448
0.52
0.75
cpDNA+morphology
2996
2504/83.6%
492/16.4%
210/7%
62
4821
412
0.59
0.82
All molecular evidence
4217
3126/74.1%
1091/25.9%
515/12.2%
62
1380
1741
0.72
0.79
All evidence
4224
3126/74%
1098/26%
522/12.3%
62
1838
1185
0.58
0.79
Phylogenetic analysis
The majority rule consensus tree resulting from the parsimony analysis of the morphological evidence (not shown),
retrieves some well-supported phylogenetic relationships, as follows: Brocchinia reducta Baker is sister to the rest of
Bromeliaceae (100 % bootstrap support); internally Bromelioideae (here represented by two species of Bromelia L.)
with 100 % of bootstrap support; Catopsis Griseb. as the sister group of Hechtia (a poorly supported relationship, 64
%), and a strongly supported clade constituted by Hechtia (a support of bootstrap of 100 %). Within Hechtia, there are
only two clades, one constituted by Hechtia tillandsioides (André) L.B. Sm. and relatives (91 % bootstrap support)
that is also retrieved in the strict consensus (not shown), and the poorly supported H. guatemalensis Mez Clade (73 %
bootstrap support). This paucity of clades identified in this parsimony analysis is not surprising considering how few
characters were included. However, the purpose of this analysis was not to resolve all the relationships of sampled
taxa, but to assess the contribution of such characters and their congruence with molecular data. The mapping of the
morphological characters on the strict consensus tree shows Hechtia to be supported by the characters: unisexual
flowers, fragrant flowers, and the simple-erect stigma with sessile stigmatic lobes, the H. tillandsioides Clade is
supported by the minutely serrulated foliar margin as well as central inflorescence, pedicellate flowers (pedicels thin),
petals reflexed with the apices retrorsely curved and pendulous fruits with papiraceous carpels, whereas the Clade H.
guatemalensis is characterized by 3/4 inferior ovary, central inflorescence as well as white petals.
The most parsimonious trees recovered by the MP analysis of the nuclear PRK region (not shown) shows no
important differences relative to that obtained through BI. In these trees, Clade B (H. tillandsioides complex) and Clade
C (H. guatemalensis complex) are sister groups (BT: 93) and they are sister to the rest of Hechtia, which is a strongly
supported relationship (BT: 99). Within Hechtia three strongly supported clades are identified: the H. glomerata Zucc.
complex (Clade D; BT= 99), the H. epigyna Harms. complex (Clade E; BT= 100), and Hechtia (Clade F; BT=94).
The best trees from the parsimony analysis of the combined plastid regions (not shown) show some relevant
differences relative to the majority rule consensus tree retrieved by the Bayesian analysis of the same regions. The most
parsimonious trees retrieve Brocchinia reducta as sister to the rest of Bromeliaceae (BT=100), which is resolved as a
polytomy. Thus, the sister group of Hechtia is not identified here. Clades B and C are resolved in the same topology as
in the Bayesian analysis. However, Clade D is not monophyletic in this analysis and Clade E is retrieved within Clade
F (rest of Hechtia included in this study). The majority rule consensus tree from the Bayesian analysis shows better
resolution than the most parsimonious trees.
Figure 2 features a comparison of a 50 % majority rule of a Bayesian inference analyses of the combined plastid
regions (left) and the nuclear PRK region (right). Both analyses retrieve Hechtia as monophyletic and strongly
supported (PP=1, both analyses). Both analyses also identify the same major clades but in different, yet not incongruent,
topologies. The PRK analysis identifies a (Pitcairnioideae(Bromelioideae(Puyoideae))) higly supported (PP=1) clade.
However, in the plastid analysis there is a basal polytomy containing Hechtioideae, Tillandsioideae, and a moderately
(PP=0.91) supported (Navioideae (Pitcairnioideae (Bromelioideae, Puyoideae))) clade (henceforth, the NPPB-clade).
Within Hechtia the nuclear PRK region recovers a highly supported (PP=0.99) sister relationship for Clade B and Clade
C. Within Hechtia, topologies for the remaining taxa are in agreement between both analyses in a highly supported
clade (Clade F) (PP=1 in the plastid analysis; PP=1 in the nuclear analysis). In all cases, a polytomy formed by three
clades (D, E, and F) is identified, each clade with the same species composition except by H. mapimiana López-Ferr.
& Espejo that does not group in Clade F (it does with plastid evidence) and a clade formed by H. myriantha and
Hechtia sp. TAMPS: Jaumave, that do not group with Clade D (as they do with the nuclear region). On the other hand,
a sister group relationship of Clade B (Clade H. tillandsioides) and the rest of Hechtia is strongly supported (BT= 98;
PP=0.99) in the plastid analysis (Figure 2, left). In the nuclear analysis, Clade B is highly supported (BT=93; PP=0.99)
as sister to Clade C.
The strict consensus parsimony tree (not shown) of combined data sets (morphology and molecular) presents
less resolution for the relationships of the large clades, but within them, there are no topological differences with the
50 % majority tree performed with BI analysis; thus we have chosen to present the Bayesian inference tree (Figure
3), including values of posterior probabilities (PP) as well as bootstrap (BT) supports for clades retrieved from the
MP analysis. In this combined analysis, the sister group of Hechtia (Clade A) is the NPPB-clade, albeit with very
low support (PP=0.57). Hechtia (Clade A) is retrieved as monophyletic and strongly supported (BT=100; PP=1) and
composed of two clades: the H. tillandsioides complex (Clade B) as sister to the rest of Hechtia, a poorly supported
relationship (PP=0.86).
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FIGURE 2. Left: A 50 % majority rule tree resulting from of a Bayesian analysis of the plastid DNA regions rpl32-trnL, ycf1(a,b).
Posterior probabilities are above the branches. Right: A 50 % majority rule tree resulting from a Bayesian analysis of the nuclear region
PRK. Posterior probabilities values are indicated above the branches. Clades are indicated with letters (A-F) and discussed in the text.
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FIGURE 3. A 50 % majority rule tree resulting from a Bayesian analysis of the chloroplast (rpl32-trnL, ycf1(a, b), nuclear PRK region,
and seven morphological characters of Hechtia. Bootstrap values are given above the branches, posterior probabilities below the branches.
Clades are indictaed with letters (A-F) and discussed in the text. The Cortes Sea (Clade CSC); Tehuantepec Isthmus Clade (TIC), Mixteca
Region Clade (MRC), and Tehuantepec-Mixteca Clade (TMC).
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Following with the results of the 50 % majority tree performed with BI of all evidence, the rest of Hechtia consists
of two clades: Clade C (BT=100; PP=1) is composed by the species in the H. guatemalensis complex, and is sister
(a poorly supported relationship (PP=0.86)) to a highly supported (BT=100; PP=1) clade which is composed of an
internal trichotomy, each clade highly supported and morphologically distinctive: the first is Clade D (BT=99; PP=1)
composed of the species in the H. glomerata complex, forming two subclades: one consisting of H. elliptica L.B. Sm.
+H. hernandez-sandovalii I. Ramírez, C.F. Jiménez & J. Treviño, the other including the rest of the complex. The
second clade in the trichotomy is Clade E (BT=100; PP=1) composed by two species: H. deceptrix I. Ramírez & C. T.
Hornung and H. epigyna; and the third, Clade F (BT=97; PP=1), with the rest of the species included in this analysis.
Internally, Clade F lacks resolution at several levels but a few clades are readily indentified. The high-elevation,
colorful H. matudae L.B. Sm. is sister (BT= 97; PP=1) to all of the other groupings within Clade F. This species
was originally thought to belong to the H. podantha Mez complex but this relationship is not supported in any of the
analyses. A few additional clades are also well-supported but hard to diagnose morphologically at this time although
geographically structured. One clade with three species (H. cordylinoides Baker (H. flexilifolia I. Ramírez & Carnevali
+H. nuusaviorum Espejo & López-Ferr.)) is highly supported (BT= 98; PP=1). Other well-supported (BT= 97; PP=
1) grouping includes H. aquamarina I. Ramírez & C.F. Jiménez, H. glauca Burt-Utley & Utley, H. lyman-smithii
Burt-Utley & Utley, H. mooreana L.B. Sm., H. oaxacana Burt-Utley, Utley & García-Mend., H. roseana L.B. Sm., H.
sphaeroblasta B. L. Rob. and H. tehuacana B.L. Rob. Another interesting, highly supported (BT= 96; PP=0.75) clade
retrieved by the analysis is that composed of the species pair H. rosea and H. meziana. However, these two species
are not retrieved as sisters in the combined Bayesian analysis of plastid DNA but they are with nuclear region PRK
(BT=97; PP=1). Hechtia iltisii, the other species with an ornithophilous or psychophily syndrome, is never sister in
any analysis of any of the two red-flowered species from the Tehuantepec area.
Results of the evolutionary reconstruction of relevant morphological characters are depicted in Figure 4. The
majority rule consensus tree emerging from the Bayesian inference analysis of the combined evidence (plastid and
nuclear regions plus structural characters) was employed to assess these evolutionary patterns. Character states
reconstructed were (Appendix 2) seven, three of which resulted synapomorphic for Hechtia, namely: simple-erect
stigma/style lacking; presence of floral fragrance (evolved in parallel in some South American Tillandsia species),
and unisexual flowers. The latter character state also shows parallel evolution in Catopsis. Another taxonomically
relevant character in the Bromeliaceae, the type of fruit, was reconstructed, and capsular fruits, such as those in
Hechtia, resulting plesiomorphic (reconstructions not shown). The character evolution reconstruction shows the SSP
architectural pattern (sensu Ramírez et al. 2014) to be symplesiomorphic in Bromeliaceae and in Hechtia. On the other
hand, the PMP architectural pattern is hypothesized to have evolved twice in Hechtia, once in Clade D, and again in
H. epigyna (Clade E) from ancestors with a SSP growth pattern. Finally, precocious-flowering rossetes (the SPFP
architectural pattern) apparently evolved at least three times within Hechtia (Clade F), most likely from SSP ancestors;
however, the lack of resolution within this clade does not allow for a more accurate reconstruction of the evolution of
this growth pattern. Inferior ovaries evolved at least twice within Bromeliaceae, once within Bromelioideae and again in
Clade E (H. deceptrix and H. epigyna), whereas a ¾ inferior ovary evolved once within Clade C (the H. guatemalensis
complex), in both cases from ancestors with superior ovaries. The reconstruction of foliar margin evolution showed
that the ancestral state of Hechtia is ambiguous. However, a serrulate foliar margin is synapomorphic for Clade B,
whereas a spiny foliar margin is either synapomorphic or symplesiomorphic for all remaining Hechtia (depending on
which ancestral state Hechtia had).
Discussion
General considerations
This is the first analysis of the internal relationships of Hechtia with a truly comprehensive data set (50 species out
of 75 species in the genus; Ramírez-Morillo et al. 2016) and evidence from sequences of both plastid and nuclear
DNA along with morphological data. The number of species included in the present analysis represents ca. 83 %
of the accepted species in Hechtia. In contrast, previous phylogenetic analyses of Bromeliaceae only included 1–4
species (Reinert et al. 2003; Crayn et al. 2004; Givnish et al. 2004, 2006, 2007; Rex et al. 2009; Barfuss et al. 2005;
Schulte et al. 2009; Horres et al. 2007; Schulte & Zizka 2008; Givnish et al. 2014). It is also noteworthy that the
sampling for this study represents all the morphological groups we have identified to date in Hechtia, including taxa
representing the three growth patterns found in the genus (sensu Ramírez et al. 2014). Furthermore, it also spans all
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of the biogeographic areas occupied by the genus in Megamexico III. The sampling includes species representing the
variation in characters of taxonomically and putatively ecological and evolutionary relevance, such as different leaf
margins and texture, flowers (pedicellate vs sessile), putative pollination syndromes, and altitudinal preferences. Thus,
the results that emerge from this analysis, expressed as well-supported relationships, can be thought of as a reflection
of phylogenetic relationships throughout the genus. However, relationships within and between some clades are still
unresolved; thus, additional evidence must be incorporated to the analysis to better assess the evolutionary history of
Hechtia.
FIGURE 4. Ancestral character state reconstructions of selected morphological characters using Maximum Parsimony, on the 50 %
majority rule tree resulting from a Bayesian analysis of morphological and molecular evidence for species of Hechtia and selected
outgroup. A. Growth pattern. B. Foliar margin. C. Ovary position. See Appendix 2 for a list of morphological characters used in the
analysis. For this, we used the consensus tree of 50 % majority of Bayesian inference using the total evidence, and the reconstruction of
the ancestral states was done through parsimony.
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Phylogenetic relationships
Sister relationships of Hechtia: Recent, well-supported phylogenetic analysis of Bromeliaceae (Givnish et al. 2014)
strongly support the notion that Hechtia is monophyletic and sister to Clade NPPB (BT= 77; PP=96). In our analysis,
however, support for a Clade NPPB-Hechtia relationship is weak (no bootstrap support and PP=0.65), a finding most
likely explained by our use of fewer DNA regions and a smaller, less representative outgroup.
Monophyly of Hechtia: All of the topologies retrieved from our analysis strongly support the monophyly of
Hechtia. These results are consistent with previous studies (i.e. Rex et al. 2009; Givnish et al. 2007, 2011, 2014), all
performed with a much smaller sampling of the genus. From the onset of the study, monophyly of Hechtia was expected
because the genus is characterized within the Bromeliaceae by a distinctive combination of features, particularly the
terrestrial, succulent habit, the unisexual, fragrant flowers, the entomophily, the dioecy, and the simple-erect stigma
with sessile stigmatic lobes (Figure 5). This aggregation of character states is unique in the Bromeliaceae, which is
a predominantly hermaphroditic clade, typically with odorless flowers, ornithophilous pollination syndromes, and a
stigma usually with a well-developed and conspicuous style. As here circumscribed, members of Hechtia are rosette
forming plants growing as terrestrials or lithophytes in volcanic, calcareous, or gypsophilous soils; their growth is
cespitose or more rarely, rhizomatous. The inflorescences are mainly central (originating from a mature rosette or from
a young one that stops its growth after blooming), or also lateral. Inflorescences are glabrous, waxy, or covered by
white indumentum. The flowers are usually sessile, or with a short, thick pedicel (which may possibly be interpreted
as an elongated receptacle holding nectariferous tissue, E. Gouda pers. comm.) or more rarely, provided with thin,
long pedicels; petals are white, green, yellow, bluish to pale lilac, or red; sepals differs in texture and color from petals.
Flowers last only one day, and both sexes produce a soft, sweet fragrance (excepting the red-flowered species). They
usually attract bees, wasps, and flies of different species, but other flower visitors such as small beetles and butterflies
are also lured by the abundant nectar and pollen produced by the flowers. Fruits are capsules with carpels of variable
texture, ranging from hard to papyraceous; the seeds are fusiform, with nothing to aid in their dispersal but a pair of
very tiny wings at both ends; this explains their low vagility and probably the high species-level endemism. Although
unisexual flowers appear to be arisen twice in Bromeliaceae according our reconstruction of ancestral states [in Catopsis
nutans (Sw.) Griseb.], this feature and dioecy are known elsewhere in the Bromeliaceae. Other Megamexican species of
Catopsis (Tillandsioideae), Aechmea mariae-reginae H. Wendl. and a single species of Androlepis Brongn. ex Houllet
are dioecious, and represent at least two independent origins of this state, since Catopsis belong to Tillandsioideae,
and Aechmea maria-reginae and Androlepis are part of the same clade within Bromelioideae (Sass & Specht 2010).
Also, unisexual flowers have been recorded in Dyckia Schult. & Schult. f. (Pitcairnioideae; Varadarajan 1986) but
in these cases, plants are monoecious, and representing an independent origin as well from those in Hechtia, since
Dyckia is well nested in Pitcairnioideae s. s. (Schütz et al. 2016); in Cryptanthus Otto & A. Dietr. there are plants with
hermaphroditic and staminate flowers, a breeding system called andromonoecy (Ramírez-Morillo & Brown 2001). Our
current understanding of phylogenetic relationships in the Bromeliaceae (e.g., Givnish et al. 2011, 2014) indicate that
flower unisexuality (and breeding systems associated with it) evolved independently several times in the family from
hermaphroditic ancestors. The evolutionary and ecological correlates of this fact are not understood at this time and
they are found in various ecosystems (terrestrial and epiphytes, xeric sites to humid forests, low to high altitudes) and
geographical areas (Megamexico III, Central America, and South America). However, it is noteworthy that all truly
dioecious taxa are native from Megamexico III and Central America. In this regard, some species are extraordinary in
being site-specific dioecious, such as Catopsis nutans, which presents perfect-flowered populations in Florida, USA
but populations of the species are dioecious in Mexico (Benzing, Luther & Bennett 2000).
The presence of floral fragrance is even more unusual in the family. All species of Hechtia produce diurnal
flowers that last but a few hours. Most species produce strong to subtly sweet aromas, as well as abundant pollen
(staminate flowers) and most commonly yellow colored nectar (both sexes). Stingless bees, as well as the introduced
Apis mellifera L. (and a few, additional opportunistic insects) are the visitors and pollinators by excellence (RamírezMorillo et al. 2008). Also, Benzing (2000) discussed the possibility of beetle pollination in Hechtia owing to the
nature of floral fragrance (e.g. aminoid odor). Furthermore, two closely related species, H. rosea and H. meziana,
along with the unrelated H. iltisii, showed a reversion: all three species feature semi-tubular corollas of reddish colors,
which fail to emit fragrances. These are most likely hummingbird or butterfly pollinated, a hypothesis yet to be
formally tested. Givnish et al. (2007) suggest that entomophily is an ancestral pollinating syndrome in the family
(recorded in Brocchinioideae, Navioideae, Lindmanioideae, Hechtioideae and Fosterella L.B. Sm. in Pitcairnioideae)
and that ornithophily evolved from ancestors with insect pollination. A few other species of Bromeliaceae feature also
fragrant flowers. For example, several species of the Diaphoranthema Beer and Phytarrhiza (Vis.) Baker subgenera of
Tillandsia L. and the recently described tillandsioid genus Lemeltonia Barfuss & W. Till, display fragrant flowers of
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Phytotaxa 376 (6) © 2018 Magnolia Press • 239
diurnal anthesis, whereas taxa such as Stigmatodon Leme, G.K. Br. & Barfuss (Barfuss et al. 2016), along with genera
and species such as Werauhia J.R. Grant and Encholirium glaziovii Mez feature highly fragrant flowers of nocturnal
anthesis that are probably moth or bat pollinated. Bromeliaceae with fragrant flowers of diurnal anthesis are even more
uncommon. Bromelia palmeri Mez, is an example where the yellow tubular flowers emit a sweet, menthol fragrance.
FIGURE 5. Features of Hechtia. A. Rhizomatous rosettes of Hechtia roseana. B. Spinose foliar margins of Hechtia iltisii. Growth patterns
(Ramírez et al. 2014): C. Hechtia malvernii with central inflorescence on mature rosette [SSP]. E. Sympodial with precacious blooming
[SPFP] in Hechtia huamelulaensis. F. Pseudomonopodial [PMP] in Hechtia schottii. D. Pistillate flower showing simple-erect with sessile
stigmatic lobes in Hechtia stenopetala. G. Staminate flowers of Hechtia schottii. H. Staminate flowers with a buttlerfly in Hechtia rosea.
I. Capsular fruits of Hechtia roseana. J. Claviform seeds of Hechtia montana. K. Almost wingless, ellipsoid seeds of Hechtia tehuacana.
L. Fusiform seeds of Hechtia aquamarina. Photograph credits: (A) Claudia Ramírez-Díaz. (C, I) K. Romero-Soler. (B, E) I. RamírezMorillo. (D) G. Romero-González. (G) G. Carnevali. (H) D. Carnevali. (F) C. Jiménez-Nah. (J, K, L) L. Can-Itzá and E. Gorocica.
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The presence of a simple erect stigma, an apomorphy of Hechtia, has also been documented in species of several
genera (Brown & Gilmartin 1989): in Cryptanthus (Bromelioideae), Brocchinia Schult. f. ex Schult. & Schult. f.
(Brocchinioideae), Brewcaria L.B. Sm., Steyerm. & H. Rob., and Cottendorfia Schult. & Schult. f. (Navioideae),
Fosterella (Pitcairnioideae), Catopsis, Guzmania Ruiz & Pav., Tillandsia, and Vriesea Lindl. (Tillandsioideae). This
type of architectural morphology translates into a reduction of the stigmatic area, which could lead, in addition to a
smaller area for pollen deposition, to a reduction of water loss (Brown & Gilmartin 1989), a condition that may be
advantageous for a group of xeric plants like Hechtia. Species that belong to these genera and which present simple
erect stigma are not all inhabitants of xeric sites, but all share bee pollinating syndromes (except perhaps the Guzmania
species, most of which have ornithophilous characters), and it would be worthwhile to study this correlation. Recently,
Barfuss et al. (2016) reported several additional architectural types in Tillandsioideae, all variations of the simple erect
morphology, with variations in the position and conformation of the stigmatic lobes. Our preliminary study of stigmatic
morphology based upon a relatively large sample of Hechtia, allowed us to identify several of the morphologies
described by Brown & Gilmartin (1989) such as simple-erect for H. nuusaviorum as well as conduplicate-erect (sensu
Leme 2009) for H. pringlei B. L. Rob. & Greenm. The small sample size of our preliminary exploration of this
character evidences its high variability within Hechtia and warrants further research. The simple-erect stigma, on the
other hand, has been reported for only a few genera besides Hechtia: Catopsis, Dyckia, Racinaea M.A. Spencer &
L.B. Sm., and Tillandsia (Varadarajan 1986; Brown & Gilmartin 1989), all of them, probably representing independent
origins of this feature. These preliminary results of stigmatic and style morphology suggests that a detailed, more
exhaustive study of stigmatic morphology in Hechtia is likely to yield a variation greater than suspected and support
the circumscription of already identified or novel groups within the genus.
Internal relationships: Internally, there are three well supported clades within Hechtia: B, C and a trichotomy
(formed by clades D, E, and F). Clade B, sister of the rest of the genus Hechtia, comprises four species corresponding
to the H. tillandsioides complex. This clade includes H. caerulea (Matuda) L.B. Sm., H. lundelliorum L.B. Sm., H.
purpusii Brandegee, and H. tillandsioides, species characterized by being rosetophilous herbs, with strict sympodial
growth, with or without a well-defined, prostrate to suberect stem (H. caerulea); older plants feature long, pendent,
narrow leaves, superficially conferring the plants a grassy aspect when seen from afar growing on vertical rocky walls
(somewhat resembling species of the genus Pitcairnia L’Hér). The leaves have minutely serrate margins; adaxially the
leaves are green, glaucous, and shiny or at the most have reddish margins whereas abaxially they are always whitelepidote; the apex is dry and often coiled. The flowers show thin pedicels; the petals are transversely convex, coiled/
reflexed, exposing the entire ovary (or pistillode), and stamens (or staminodes). The petal color varies from white (as
in H. purpusii and H. lundelliorum) to pink (H. tillandsioides), lilac and caerulescent (as in H. caerulea), thin-textured
petals; the fruits are erect when immature, then the pedicel bends down and the fruits are pendulous upon maturity
with carpels becoming papiraceous and releasing minute seeds of ca. 4 mm long with two apical wings. Most species
from this clade are terrestrial but some grown on rocky volcanic soils (as H. caerulea). They occur in low caducifolious
forests, in some places always on vertical walls (as H. lundelliorum). This clade is distributed in the Transmexican
Volcanic Belt, the Sierra Madre Oriental, and the Veracruzan provinces, always on the Gulf of Mexico slope (PechCárdenas 2015; Romero-Soler 2017). This clade is well characterized by its serrulate leaves, pedicelled flowers, these
with transversely convex petals, and fruits pendulous with papiraceous carpels; its monophyly is also well supported
by molecular features, along with a fairly circumscribed biogeographical distribution.
The second clade, Clade C, is formed by species belonging to the so-called Hechtia guatemalensis complex,
distributed in the southern portion of Megamexico III, in the Pacific Lowlands, Veracruzan, Mosquito, and the Chiapas
Highland Provinces (in Belize [Holst et al., 2017], Guatemala, Honduras, El Salvador, and Nicaragua). This species
aggregation is characterized by rosettes with strict sympodial growth, serrate leaves, very short spines, these hard and
rigid and homogenous in size and shape along the margin, or when long, soft and flexible; upon exposure to the sun,
the foliar blades develop red pigments resulting in a green-red pattern. The foliar surfaces are lustrous adaxially, whitelepidote abaxially. The flowers have green or red sepals, the corolla is spreading and the petals form a semi-cup; the
star-like flowers have white petals and a ¾ inferior ovary; some species (H. guatemalensis) have pendulous mature
fruits. The inflorescences develop quickly but flowers open a few at a time, thus making the blooming period to last
for almost a month, more than any other species group in the genus where the inflorescence usually last just a week.
This clade is diagnosed by a combination of characters: central inflorescences, flowers with ovary ¾ inferior, white
flowers, and a distribution in Central America only, south of Motagua River close to the Guatemalan-Honduras border
extending to northern Nicaragua. This clade includes the following species: H. malvernii Gilmartin, H. dichroantha
Donn. Sm., and H. guatemalensis.
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A third clade, Clade D, the so-called H. glomerata complex, includes all of the species with lateral inflorescences
(with the exception of H. epigyna, discussed below), all floral parts are white lepidote and the petals are white. Lateral
inflorescences are unusual and phylogenetically scattered in Bromeliaceae. They have been recorded in species of
Greigia Regel and Disteganthus Lem. (Bromelioideae), and Dyckia (Pitcairnioideae; Benzing 2000), as well as
occasionally in Tillandsioideae (e.g. Tillandsia complanata Benth.). Beyond the lateral inflorescences, species in this
clade share several morphological features (Jiménez-Nah 2014): inflorescences are variously white-lepidote and the
short-pedicelled flowers have always petals white in both sexes (except H. pretiosa Espejo & López-Ferr. that bears pink
to magenta petals). The taxa of this clade are distributed in the Gulf of Mexico drainage in the Veracruzan, Tamaulipan,
Yucatecan, and Sierra Madre Oriental biogeographical provinces, with a few species ranging into the neighboring
provinces of the Mexican Plateau (H. argentea Zucc., H. glomerata, and probably H. texensis S. Watson, this last one
not included in this analysis). An additional 3–4 undescribed species are known from the Chiapas Highlands provinces
(Chiapas, as well as Honduras and Guatemala). The taxonomy of this group is highly complex and species are difficult
to delimit and identify. Among the factors causing this complexity are the polycarpic growth of their rosettes; thus
plants start to flowering when vegetatively still immature and coexist with much older, mature specimens bearing
larger rosettes that have produced many, increasingly longer, more massive inflorescences. This results in populations
containing plants on an immense array of sizes and degree of inflorescence branching. Hence, vegetative variation
of fertile plants, at least sizes, may overlap among the closely related species, with the larger plants of vegetatively
reduced species overlapping the dimensions of smaller plants of vegetatively large taxa. To make things worse, several
species of the complex are only known from fragmentary specimens, rendering herbarium taxonomy a nightmare.
Most of the diagnostic features of species are rosette characters and flower part sizes, along with fruit characters and
geographical distribution.
Clade E is formed by Mexican species with inferior ovary: Hechtia epigyna from the Tamaulipas biogeographical
province, and H. deceptrix, recently described from Hidalgo (known from the Sierra Madre Oriental Province and
neighboring areas of the Transmexican Volcanic Belt Province). Hechtia epigyna differs from H. deceptrix (RamírezMorillo et al. 2015) in its pseudomonopodial growth pattern, lateral inflorescence, flowers with lilac petals whereas
H. deceptrix features flowers with white-greenish petals, strict sympodial growth pattern with central inflorescence.
The placement of these two species in a well-supported clade, strongly suggests that lateral inflorescence evolved
independently twice in Hechtia. Inferior ovary, on the other hand, evolved only in this clade within the genus, as well
as independently in subfamily Bromelioideae.
Clade F is a strongly supported aggregation containing most of Hechtia taxa (40 % of formally described species)
and shows low resolution of internal phylogenetic relationships. Of the several morphological complexes characterized
at the onset of this study, some resulted non-monophyletic. One such group is the so-called H. podantha complex. This
is composed of species occurring at relatively high elevations of the Mexican Plateau that have central inflorescences
emerging from a fully grown rosette (SSP growth pattern) and often feature conspicuously inflated inflorescence bracts
(primary bracts) and short branches, usually shorter or as long as the primary bract length. Examples of such taxa are
H. matudae, H. podantha, H. roseana, and H. tehuacana, all of which inhabit xerophytic shrublands, mostly at the
higher elevations of the Mexican Plateau and Mexican Transvolcanic Belt. The species previously referred to the H.
podantha complex were retrieved scattered within several clades within Clade F, with no structural or biogeographical
evidence supporting its monophyly. Another example is the H. rosea complex, which encompasses the three species
with tubular, red, fragrantless flowers, whose species fell in different clades: Hechtia rosea is sister to H. meziana
(nuclear PRK and total evidence analyses) whereas the third species with this kind of floral morphology, H. iltisii
is never retrieved as related to the species pair. However, the phylogenetic structure within Clade F features the
phenomenon of geographically restricted clades, a recurrent theme in the evolution of Hechtia and other plant groups.
Each clade represents a morphologically and ecologically diverse assemblage of species that invaded a particular
area and radiated within it. There, they apparently would have filled several morphological space, pollination, and
life history niches, often duplicating the patterns found in of different other clades of Clade F in different areas of
Megamexico III. A discussion of this follows, clade by clade.
One of the clades retrieved by the analysis is that composed by several taxa for NW Mexico, here referred to as
“The Cortes Sea Clade” (CSC). This clade, represented in the analysis by six species, occurs around the mentioned
sea in the states of Sonora, Baja California, Baja California Sur, Sinaloa, Nayarit, Durango, and Chihuahua. Central
inflorescences are the norm here. A possible instance of hummingbird pollination was “invented” (evolved) within this
clade, in H. iltisii, whereas the rest of the taxa feature the standard, bee pollinated, white flowers. Similarly, features
of the H. podantha syndrome (henceforth, HPS) are found in H. mapimiana López-Ferr. & Espejo and H. subalata
L.B. Sm., both high-elevation species. It seems that the HPS has been selected for dry, cold places and results in an
242 • Phytotaxa 376 (6) © 2018 Magnolia Press
RAMÍREZ-MORILLO ET AL.
inflorescence with dense glomerules of flowers with fleshy (often yellow or green) petals, partially enveloped by
inflated peduncle bracts. Presumably, this combination of characters affords protection to both young buds and flowers
against dry and cold weather, particularly from frosts. Thus, this inflorescence structure is found in several, unrelated
clades of Hechtia that grow at such high elevations.
A second clade is composed of taxa that occur in the vicinity of the Tehuantepec Isthmus (TIC). All are inhabitants
of hot, seasonally dry forests and feature the SPFP (sympodial with precocious-flowering pattern, SPFP) architecture.
This growth pattern is here hypothesized as a way to gain a head-start with the flowering period and, later on, take
advantage of the rainy season to release the seeds. The SPFP pattern is only found in Hechtia species from dry
areas. Two species of this clade (H. rosea and H. meziana) feature presumably ornithophilous flowers, an independent
“invention” (evolution) of this kind of floral model. Hechtia stenopetala Klotzsch, the type of the genus, is a member
of this clade and the only one that grows on the Gulf of Mexico drainage in the dry areas of central Veracruz. The
Tehuantepec Isthmus has served in the past as a two-way bridge for the passage of taxa from the Atlantic drainage to
the Pacific watershed and vice versa. There are many examples of this mixture of floras (e.g. Pérez-García & Hágsater
2012). We will provide some examples from the Bromeliaceae. Tillandsia ionantha Planch. is a member of a Pacificdrainage clade of Tillandsia but there are populations in central Veracruz. On the other hand, Tillandsia streptophylla
Schweidw. ex E. Morren is widespread on the Atlantic drainage from Honduras to Central Veracruz. However, there
are isolated populations of the species in the southern area of the Tehuantepec Isthmus, particularly in the Chimalapas
area.
Another group within Hechtia, the Mixteca Region Clade (MRC Clade), is composed of several species that
occur on both sides of the Central Valley of Oaxaca, particularly in the Mixteca Region. These species occur at
relatively high elevations and in more mesic places than those of the previous clades, some occurring at the margins
and on rocky outcrops of mesophilous forests. Albeit most taxa of this clade feature the SPFP architecture, at least
two taxa feature SSP architecture: H. pringlei growing at intermediate to high elevations around the Central Valley of
Oaxaca and H. pumila Burt-Utley & Utley, that grows in thorn scrub vegetation at middle elevations in the Mexican
State of Guerrero. Within this clade, a subclade composed of three taxa, H. cordylinoides, H. nuusaviorum, and H.
flexilifolia is noteworthy by displaying alternative strategies of niche occupation associated with cladogenesis. H.
cordylinoides is sister to the other two species and morphologically very similar to H. flexilifolia whereas the sympatric
H. nuusaviorum and H. flexilifolia are morphologically very different and grow side by side, even flowering more or
less simultaneously.
A final clade within Hechtia is that composed of taxa restricted to the relatively high elevation, extremely dry
environments in the Tehuacán area and neighboring high western Mixteca Region (TMC). Species of this clade
mostly display the SPFP growth pattern. However, H. roseana, restricted to the vicinities of the Valley of Tehuacán,
has apparently evolved independently the Hechtia podantha syndrome. This clade is extremely variable in terms of
vegetative structure. Species such as H. lyman-smithii are vegetatively reduced, densely cespitose, succulent, whereas
H. roseana is a large plant that grows by means of elongated rhizomes that ramble among the surrounding vegetation
searching for appropriate microniches where a new central-flowering rosette will root. At the other extreme of the
variation is the gracile H. mooreana, which has an elongated, erect stem with the basic SPFP growth pattern. This clade
is an exceptional example of the evolutionary potential and plasticity of Hechtia.
Conclusions
This study, with the largest taxonomic sampling of Hechtia to date, and with the use of plastid and nuclear DNA
markers and morphological characters, provides conclusive evidence for the monophyly of Hechtia, and for it being
composed of several highly supported clades.
At this time it is uncertain what part of Megamexico was first invaded by the ancestors of Hechtia. However, as
suggested by Givnish et al. (2011) it is most likely it happened either through long-range dispersal from the West Indies
or via the southern Isthmus of Panama ca. 4.4–1.3 Ma. Regardless, it becomes clear that from the original point of
invasion they radiated to occupy multiple biogeographical and ecological spaces in what is now Megamexico. In the
meanwhile, they diversified morphologically and increased in species numbers. Today they consist in approximately
75 species-level-taxa. Nowadays, they grow from Nicaragua at its southern limits northward to Texas. In the course of
its evolution, the biogeographically correlated phylogenetic structure of the genus suggests that particular regions were
invaded at particular times and geographically confined smaller, separate radiations occurred, resulting in repeated
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Phytotaxa 376 (6) © 2018 Magnolia Press • 243
“inventions” (evolution) of critical evolutionary themes associated with the invasion of dry, highly seasonal climates,
or cooler areas subject to frosts. Simultaneously, exploration of novel pollinations systems may have also played a
role in the diversification of the genus. Speciation patterns suggests a mixture of niche conservatism and the creation
of evolutionary novelties as concurrent or alternative evolutionary forces directing the diversification of the genus.
Further ongoing macro-evolutionary research, with the inclusion of more taxa, more molecular markers, and structural
characters, will help clarify the chronology of these evolutionary events and analyze the sequence of appearance of
apomorphic novelties.
Acknowledgments
For assistance during field work in Mexico: Jacinto Treviño, Evelyn Rios, Laura Rodríguez, Sergio Terán, Gonzalo
Guerrero, Luis Martínez, Demetria Mondragón, Prisciliano Flores, José Luis Chávez, Gerardo Salazar, Carolina
Granados, María Cruz Flores, Adolfo Espejo, Javier García, Francisco Lorea, Carlos Durán, Ana Rosa López-Ferrari,
Aniceto Mendoza, Jacqueline Ceja, Carlos Jiménez-Nah, Gregorio Castillo, Brian Sidoti, Virginia Rebolledo, Julián
Bueno, Sofía Bueno, Ian Carnevali, Víctor Carnevali, Débora Carnevali, Oswaldo Suárez, William Cetzal, Sergio
Zamudio, Luis Hernández Sandoval, Manuel Pool, Guadalupe Chuc, Francisco Chi, Filogonio May, Pablo Carrillo,
Francisco Santana, Alejandro Zabalgoitia, Claudia Ramírez, Manuel González, Ivan Tamayo; in Honduras: Iliam and
Daniel Rivera, Hermes Vega, Lilian Ferrufino, Paul and Margarita House, and Víctor Bocanegra; in Guatemala: Edgar
Mó. The following people provided dried material on silica gel or help to obtain it: Pamela Hyatt, Dan Kinnard, Eloise
Lau, Robert Kopstein, Ángel Lara, Raquel Monteiro, Rafaela Forzza, Claudine Mynssen, Andy Siekkinen, the Marie
Selby Botanical Gardens and the Missouri Botanical Gardens. For maintaining the living collections at CICY: Clarisa
Jiménez and Lilia Carrillo. To Lilia Can-Itzá and Alejandro Gorocica for images of seeds on the SEM. The senior
author is indebted to the Elizabeth Bascom Fellowship and the Missouri Botanical Garden, the DAAD-ANUIES,
Klarff Foundation, and Andrew Mellon Foundation, for financial support to study Bromeliaceae collections at herbaria
in USA and Europe. To CONACyT for financial support (projects 67050 and 183281 to the first author). Thanks to
curators of herbaria ASU, B, BIGU, CHAPA, CICY, EAP, ENCB, F, GH, HGOM, HUH, IBUG, IZTA, K, LAGU, LL,
MEXU, MHES, MICH, MO, NY, PH, QMEX, SEL, TEFH, TEX, UAMIZ, US, W, WU, XAL, ZEA for allowing us
borrowing their material. For access to databases and herbarium voucher images our thanks to the curators of herbaria
B, CICY, MO, UAMIZ, particularly to Mary Merello, Jim Solomon, Gerrit Davidse, Tom Wendt, Adolfo Espejo, and
Silvia Hernández-Aguilar. Special thanks to Gustavo Romero (HUH), Walter Till (WU), Rusty Russell (US) and the
Peter Raven Library Staff at Missouri Botanical Garden, for their support on getting loan of herbarium specimens as
well as specialized literature on Hechtia. We also acknowledge Walter Till, an anonymous reviewer and Eric Gouda,
whose comments and suggestions improved this paper.
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248 • Phytotaxa 376 (6) © 2018 Magnolia Press
RAMÍREZ-MORILLO ET AL.
Appendix 1. Information for samples of species of Hechtia and the outgroup. Voucher information is listed as
follows: taxon name, country, state or department, and locality, collector’s name and number, herbarium abbreviation.
Herbarium abbreviations according to Thiers, B. (2018). GenBank numbers appear in the following order: rpl32-trnL,
ycf1a, ycf1b, PRK; a dash indicates that the locus was not sequenced for the specimen. Sequences generated in this
study are indicated with an asterisk*. Plants in cultivation without voucher are indicated as (l).
Brocchinia reducta Baker. Venezuela, A.M. Piliackas s/n (RB), MF74097*/MF74103*/ MF74109*/MF74092*.
Bromelia hemispherica Lam. Mexico, Jalisco, I. Ramírez 1806 (CICY), MF740978*/ MF741038*/MF741097*/
MF740921*.
Bromelia karatas L. Mexico, Yucatán, I. Ramírez 1805 (CICY), MF740980*/MF741039*/ MF741098*/
MF740922*.
Catopsis nutants (Sw.) Griseb. Mexico, s/l, J. Pinzón s/n (CICY), MF740981*/MF741040*/MF741099*/
MF740923*.
Cottendorfia florida Schult. f. Brazil, s/l, S. C. de Sant ìAna 3692 (RB), MF740982*/MF741041*/ MF741100*,_.
Encholirium magalhaesii L.B. Sm. Brazil, s/l, M. Moura 36 (RB), MF740983*, _ , MF741101*/ MF740924*.
Lindmania longipes (L.B. Sm.) L.B. Sm. Venezuela, T. Givnish s.n. (WIS), HQ913783, _ , _ , _ .
Lindmania guianensis (Beer) Mez. Venezuela, Bolívar, W. Till et al. 16018a (WU), _ , X753760/ KX753760, _ .
Pitcairnia breedlovei L.B. Sm. Mexico, Chiapas, I. Ramírez 957 (CICY), MF741034*/MF741092*/ MF741151*/
MF740974*.
Puya mirabilis (Mez) L.B. Sm. Argentina, s/l, G. Carnevali s/n (CICY), MF741035*/ MF741093*/ MF741152*/
MF740975*.
Tillandsia dasyliriifolia Baker. Mexico, Yucatán, I. Ramírez s/n (CICY), MF741036*/ MF741094*/ MF741153*/
MF740976*.
Tillandsia limbata Schltdl. Mexico, Veracruz, I. Ramírez 1464 (CICY), KU848483/MF741095*/ MF741154*/
MF740977*.
Hechtia aquamarina I. Ramírez & C.F. Jiménez. Mexico, Puebla, I. Ramírez 1283 (CICY), MF740984*/ MF741042*/
MF741102*/ MF740925*.
Hechtia caerulea (Matuda) L.B. Sm. Mexico, Mexico, I. Ramírez 1516 (CICY), MF740985*/ MF741043*/ MF741103*/
MF740926*.
Hechtia cordylinoides Baker. Mexico, Oaxaca, I. Ramírez 1441 (CICY), MF740986*/ MF741044*/ MF741104*/
MF740927*.
Hechtia deceptrix I. Ramírez & C.T. Hornung. Mexico, Hidalgo, I. Ramírez 1723 (CICY), MF740987*/ MF741045*/
MF741105*/ MF740928*.
Hechtia dichroantha Donn. Sm. Guatemala, K. Romero 1169 (CICY), MF740988*/ MF741046*/ MF741106*, _ .
Hechtia edulis I. Ramírez, Espejo & López-Ferr. Mexico, Chihuahua, I. Ramírez 1326 (CICY), MF740989*/
MF741047*/ MF741107*/ MF740929*.
Hechtia elliptica L.B. Sm. Mexico, Coahuila, I. Ramírez 1347 (CICY), MF740990*/ MF741048*/ MF741108*/
MF740930*.
Hechtia epigyna Harms. Mexico, Tamaulipas, I. Ramírez 1956 (CICY), MF740991*/ MF741049*/ MF741109*/
MF740931*.
Hechtia flexilifolia I. Ramírez & Carnevali. Mexico, Oaxaca, G. Carnevali 7136 (CICY), MF740992*/ MF741050*/
MF741110*/ MF740932*.
Hechtia fosteriana L.B. Sm. Mexico, Oaxaca, I. Ramírez 1747 (CICY), MF740993*/ MF741051*/ MF741111*/
MF740933*.
Hechtia gayorum L.W. Lenz. Mexico, Baja California, I. Ramírez 2214 (l), MF740994*/ MF741052*/ MF741112*/
MF740934*.
Hechtia ghiesbreghtii Lem. Mexico, Chiapas, G. Carnevali 7488 (CICY), MF740995*/ MF741053*/MF741113*/
MF740935*.
Hechtia glauca Burt-Utley & Utley. Mexico, Michoacán, I. Ramírez 2215 (l), MF740996*/MF741054*/ MF741114*/
MF740936*.
Hechtia glomerata Zucc. Mexico, Hidalgo, I. Ramírez 1495 (CICY), MF740997*/ MF741055*, _ , MF740937 *.
Hechtia guatemalensis Mez. Honduras, I. Ramírez 1838 (CICY), MF740998*/ MF741056*/ MF741115*/
MF740938*.
Hechtia hernandez-sandovalii I. Ramírez, C.F. Jiménez & J. Treviño. Mexico, Querétaro, I. Ramírez 1610 (CICY),
PHYLOGENETICS OF HECHTIA
Phytotaxa 376 (6) © 2018 Magnolia Press • 249
MF740999*/ MF741057*/MF741116*/MF740939*.
Hechtia iltisii Burt-Utley & Utley. Mexico, Jalisco, I. Ramírez 1937 (CICY), MF741000*/MF741058*/ MF741117*/
MF740940*.
Hechtia isthmusiana Burt-Utley. Mexico, Oaxaca, I. Ramírez 1536 (CICY), MF741001*/ MF741059*/MF741118*/
MF740941*.
Hechtia ixtlanensis Burt-Utley. Mexico, Oaxaca, I. Ramírez 1379 (CICY), MF741002*/ MF741060*/ MF741119*/
MF740942*.
Hechtia lepidophylla I. Ramírez. Mexico, Querétaro, I. Ramírez 1503 (CICY), MF741003*/ MF741061*/ MF741120*/
MF740943*.
Hechtia lundelliorum L.B. Sm. Mexico, San Luis Potosí, I. Ramírez 1491 (CICY), MF741004*/ MF741062*/
MF741121*/ MF740944*.
Hechtia lyman-smithii Burt-Utley & Utley. Mexico, Oaxaca, I. Ramírez 1038 (CICY), MF741005*/ MF741063*/
MF741122*/ MF740945*.
Hechtia malvernii Gilmartin. Honduras, I. Ramírez 1842 (CICY), MF741006*/MF741064*/ MF741123*/
MF740946*.
Hechtia mapimiana López-Ferr. & Espejo. Mexico, Durango, I. Ramírez 1317 (CICY), MF741007*/ MF741065*/
MF741124*/MF740947*.
Hechtia matudae L.B. Sm. Mexico, Morelos, I. Ramírez 1918 (l), MF741008*/MF741066*/ MF741125*/
MF740948*.
Hechtia melanocarpa L.B. Sm. Mexico, Guerrero, I. Ramírez 2217 (l), MF741009*/ MF741067*/ MF741126*/
MF740949*.
Hechtia meziana L.B. Sm. Mexico, Chiapas, I. Ramírez 962A (CICY), MF741010*/ MF741068*/ MF741127*/
MF740950*.
Hechtia michoacana Burt-Utley, Utley & García-Mend. Mexico, Michoacán, I. Ramírez 1105 (CICY), MF741011*/
MF741069*/MF741128*/MF740951*.
Hechtia montana Brandegee. Mexico, s/l, I. Ramírez 2216 (l), MF741012*/MF741070*/ MF741129*/MF740952*.
Hechtia mooreana L.B. Sm. Mexico, Guerrero, I. Ramírez 1976 (CICY), MF741013*/ MF741071*/ MF741130*/
MF740953*.
Hechtia myriantha Mez. Mexico, Veracruz. I. Ramírez 1462 (CICY), MF741014*/ MF741072*/ MF741131*/
MF740954*.
Hechtia nuusaviorum Espejo & López-Ferr. Mexico, Oaxaca, G. Carnevali 7133 (CICY), MF741015*/ MF741073*/
MF741132*/ MF740955*.
Hechtia oaxacana Burt-Utley, Utley & García-Mend. Mexico, Oaxaca, I. Ramírez 1546 (CICY), MF741016*/
MF741074*/ MF741133*/MF740956*.
Hechtia podantha Mez. Mexico, Hidalgo, I. Ramírez 1479 (CICY), MF741017*/MF741075 */
MF741134*/
MF740957*.
Hechtia pretiosa Espejo & López-Ferr. Mexico, Guanajuato, I. Ramírez 2216 (l), MF741018*/MF741076*/
MF741135*/MF740958*.
Hechtia pringlei B.L. Rob. & Greenm. Mexico, Oaxaca, I. Ramírez 1442 (CICY), MF741019 * / M F 7 4 1 0 7 7 * /
MF741136*/MF740959*.
Hechtia pumila Burt-Utley & Utley. Mexico, Guerrero, I. Ramírez 1742 (CICY), MF741020*/ MF741078*/
MF741137*/MF740960*.
Hechtia purpusii Brandegee. Mexico, Veracruz, I. Ramírez 787 (CICY), MF741021*/ MF741079*/ MF741138*/
MF740961*.
Hechtia rosea E. Morren ex Baker. Mexico, Oaxaca, I. Ramírez 924 (CICY), MF741022*/MF741080*/ MF741139*/
MF740962*.
Hechtia roseana L.B. Sm. Mexico, Puebla, I. Ramírez 1293 (CICY), MF741023*/ MF741081*/ MF741140*/
MF740963*.
Hechtia schottii Baker. Mexico, Yucatán, I. Ramírez 529 (CICY), MF741024*/MF741082*/ MF741141*/
MF740964*.
Hechtia sphaeroblasta B.L. Rob. Mexico, Oaxaca, G. Carnevali 7152 (CICY), MF741029*/ MF741087*/MF741146*/
MF740969*.
Hechtia stenopetala Klotzsch. Mexico, Veracruz, I. Ramírez 1269 (CICY), MF741030*/ MF741088*/MF741147*/
MF740970*.
250 • Phytotaxa 376 (6) © 2018 Magnolia Press
RAMÍREZ-MORILLO ET AL.
Hechtia subalata L.B. Sm. Mexico, Durango, I. Ramírez 1314 (CICY), MF741031*/ MF741089*/ MF741148*/
MF740971*.
Hechtia tehuacana B.L. Rob. Mexico, Puebla, I. Ramírez 1566 (CICY), MF741032*/ MF741090*/ MF741149*/
MF740972*.
Hechtia tillandsioides (André) L.B. Sm. Mexico, Puebla, I. Ramírez 1475 (CICY), MF741033*/ MF741091*/
MF741150*/MF740973*.
Hechtia sp. 1, Mexico, Chiapas, Comitán, J. Pinzón 234 (CICY), MF741025*/ MF741083*/MF741142*/
MF740965*.
Hechtia sp. 2, Mexico, Guanajuato, Xichú, I. Ramírez 1525 (CICY), MF741026*/ MF741084*/MF741143*/
MF740966*.
Hechtia sp. 3, Mexico, Tamaulipas, Jaumave, I. Ramírez 1607 (CICY), MF741027*/ MF741085*/MF741144*/
MF740967*.
Hechtia sp. 4, Mexico, Tamaulipas, Salto del Tigre, I. Ramírez 1599 (CICY), MF741028*/ MF741086*/MF741145*/
MF740968*.
PHYLOGENETICS OF HECHTIA
Phytotaxa 376 (6) © 2018 Magnolia Press • 251
Appendix 2. Matrix of morphological characters, with characters states and codification for all taxa included in the
analysis.
Taxon/Character
and character state
codification
Brocchinia reducta
Bromelia
hemispherica
Bromelia karatas
Catopsis nutans
Cottendorfia florida
Encholirium
magalhaesii
Lindmania
guianensis
Lindmania longipes
Pitcairnia breedlovei
Puya mirabilis
Tillandsia
dasyliriifolia
Tillandsia limbata
Hechtia aquamarina
Hechtia caerulea
Hechtia
cordylinioides
Hechtia deceptrix
Hechtia dichroantha
Hechtia edulis
Hechtia elliptica
Hechtia epigyna
Hechtia felixliifolia
Hechtia fosteriana
Hechtia gayorum
Hechtia ghiesbreghtii
Hechtia glauca
Hechtia glomerata
Hechtia
guatemalensis
Hechtia hernandezsandovalii
Hechtia iltisii
Hechtia isthmusiana
Hechtia ixtlanensis
Hechtia lepidophylla
Hechtia lundelliorum
Hechtia lymansmithii
Hechtia malvernii
Hechtia mapimiana
Hechtia matudae
Hechtia melanocarpa
Hechtia meziana
Hechtia michoacana
Hechtia montana
Hechtia mooreana
Hechtia myriantha
Hechtia nuusaviorum
Hechtia oaxacana
Growth
pattern: (0)
SSP; (1)
SPFP; (2)
PMP
0
0
Foliar margin: (0) Style: (0)
entire; (1) serrulate; present; (1)
(2) spiny; (3)
absent
denticulate
Ovary position:
(0) superior; (1)
inferior; (2) partially
inferior
Floral
fragrance:
(0) absent;
(1) present
Fruit
type: (0)
berry; (1)
capsule
0
2
0
0
2
1
0
0
1
0
Floral
sex: (0)
bisexual;
(1)
unisexual
0
0
0
0
0
0
2
0
0
2
0
0
0
0
1
0
0
0
0
0
¿
0
0
1
1
1
0
0
0
0
0
2
0
0
¿
1
0
0
0
0
0
2
0
3
0
0
0
0
0
0
0
0
0
¿
0
0
0
1
1
1
1
0
0
0
0
0
1
0
1
0
2
1
2
0
1
1
1
0
0
0
0
0
1
1
1
1
1
1
1
0
1
1
1
0
0
0
2
2
1
1
0
2
1
2
0
2
2
2
2
2
2
2
2
2
2
2
2
1
1
1
1
1
1
1
1
1
1
1
1
1
2
0
0
1
0
0
0
0
0
0
2
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
0,1
1
1
1
1
2
2
1
0
1
1
1
0
1
1
2
0
1
2
2
2
2
1
2
1
1
1
1
1
1
0
0
0
0
0
0
0
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
0
0
0
0
1
1
0
1
2
1
0
2
2
2
2
2
2
2
2
2
2
2
1
1
1
1
1
1
1
1
1
1
1
2
0
0
0
0
0
0
0
0
0
0
1
1
1
1
0
1
1
1
1
1
1
252 • Phytotaxa 376 (6) © 2018 Magnolia Press
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
...continued on the next page
RAMÍREZ-MORILLO ET AL.
Appendix 2. (Continued)
Taxon/Character
and character state
codification
Hechtia podantha
Hechtia pretiosa
Hechtia pringlei
Hechtia pumila
Hechtia purpusii
Hechtia rosea
Hechtia roseana
Hechtia schottii
Hechtia
sphaeroblasta
Hechtia stenopetala
Hechtia subalata
Hechtia tehuacana
Hechtia tillandsioides
Hechtia sp. CHIS:
Comitán
Hechtia sp. GTO:
Xichú
Hechtia sp. TAMPS:
Jaumave
Hechtia sp. TAMPS:
Salto
Growth
pattern: (0)
SSP; (1)
SPFP; (2)
PMP
0
2
0
0
0
1
0
2
0
Foliar margin: (0) Style: (0)
entire; (1) serrulate; present; (1)
(2) spiny; (3)
absent
denticulate
Ovary position:
(0) superior; (1)
inferior; (2) partially
inferior
Floral
fragrance:
(0) absent;
(1) present
Fruit
type: (0)
berry; (1)
capsule
2
2
2
2
1
2
2
2
2
1
1
1
1
1
1
1
1
1
0
0
0
0
0
0
0
0
0
1
1
1
1
1
0
1
1
1
1
1
1
1
1
1
1
1
1
Floral
sex: (0)
bisexual;
(1)
unisexual
1
1
1
1
1
1
1
1
1
1
0
0
0
2
2
2
2
1
2
1
1
1
1
1
0
0
0
0
0
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
2
2
1
0
1
1
1
2
2
1
0
1
1
1
2
2
1
0
1
1
1
PHYLOGENETICS OF HECHTIA
Phytotaxa 376 (6) © 2018 Magnolia Press • 253