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Botanical Sciences

versión On-line ISSN 2007-4476versión impresa ISSN 2007-4298

Bot. sci vol.100 no.2 México abr./jun. 2022  Epub 22-Mar-2022

https://doi.org/10.17129/botsci.2893 

Systematic

Systematic study and niche differentiation of the genus Aporocactus (Hylocereeae, Cactoideae, Cactaceae)

Estudio sistemático y diferenciación de nicho del género Aporocactus (Hylocereeae, Cactoideae, Cactaceae)

1 Jardín Botánico, Instituto de Biología, Universidad Nacional Autónoma de México, CDMX, México.

2 Posgrado en Ciencias Biológicas, Instituto de Biología, Universidad Nacional Autónoma de México, CDMX, México.

3CONACYT-Laboratorio Nacional de Identificación y Caracterización Vegetal, Departamento de Botánica y Zoología, Centro Universitario de Ciencias Biológicas y Agropecuarias, Universidad de Guadalajara, Zapopan, México.

4Herbario Luz María Villarreal de Puga, Departamento de Botánica y Zoología, Centro Universitario de Ciencias Biológicas y Agropecuarias, Universidad de Guadalajara, Zapopan, México.


Abstract

Background:

Aporocactus is an epiphytic or saxicolous genus that is endemic to Mexico and has a distribution restricted to cloud forests and pine-oak forests. As with many cacti, Aporocactus presents taxonomic conflicts, especially regarding species delimitation, since five species in this genus have been described and accepted by some authors, while others accept only two species.

Questions:

How many species comprise Aporocactus? What are their relationships? Do these species show differences in their climatic preferences?

Studied species:

The five putative species in Aporocactus were investigated.

Study site and dates:

This study was conducted in 2015 and 2016. The collection sites were in Hidalgo, Puebla, Querétaro, Veracruz, and Oaxaca states, Mexico.

Methods:

In this study, phylogenetic analyses were performed using chloroplast DNA markers from different Aporocactus populations and related genera, and ecological niche modeling techniques were also employed.

Results:

The phylogenetic analyses indicated that Aporocactus is composed of only two species: A. flagelliformis and A. martianus. Additionally, the phylogenetic analyses corroborated that Aporocactus is an early diverging group related to Weberocereus and Selenicereus. Finally, niche modeling and niche identity testing indicated that the niches of the two species of Aporocactus are significantly differentiated and niches are more different than would be expected by chance.

Conclusions:

Despite being a genus with only two species, Aporocactus represents a useful model for investigating such topics as the ecology of pollination, genetic populations, and flower development to characterize the evolution of these specialized cacti.

Keywords: cpDNA phylogeny; epiphytic cacti; niche differentiation; rat-tail cactus; species delimitation

Resumen

Antecedentes:

Aporocactus es un género epifito o saxícola, endémico de México, con una distribución restringida a bosque mesófilo y de pino-encino. Como otras cactáceas, Aporocactus presenta conflictos taxonómicos, especialmente en la delimitación de especies, con cinco nombres descritos y aceptadas por algunos autores, pero otros solo aceptan dos especies.

Preguntas:

¿Cuántas especies incluye Aporocactus? ¿Cuáles son sus relaciones filogenéticas? ¿las especies muestran diferencias en sus preferencias climáticas?

Especies estudiadas:

Cinco especies putativas de Aporocactus.

Lugar de estudio y fechas:

Estudio realizado entre 2015 y 2016. Los sitios de colecta fueron los estados de Hidalgo, Puebla, Querétaro, Veracruz y Oaxaca, México.

Métodos:

El estudio incluyó análisis filogenético utilizando marcadores de ADN de cloroplasto de diferentes poblaciones de Aporocactus y géneros relacionados, así como técnicas de modelado de nicho ecológico.

Resultados:

El análisis filogenético mostró que Aporocactus está compuesto por dos especies: A. flagelliformis y A. martianus; los análisis filogenéticos corroboraron que Aporocactus diverge tempranamente y que está relacionado con Weberocereus y Selenicereus. Finalmente, el modelado y la prueba de identidad de nicho indicaron que los nichos de ambas especies de Aporocactus están significativamente diferenciados y son más diferentes de lo que se esperaría por azar. Esto indica que las especies muestran un conservadurismo de nicho.

Conclusiones:

Se reconocen solo dos especies para Aporocactus, el cual representa un modelo interesante para estudiar la ecología de la polinización, genética de poblaciones, desarrollo floral, entre otros temas, con el fin de comprender la evolución de estas cactáceas especializadas.

Palabras clave: cactácea epífita; cactus cola de rata; diferenciación de nicho; delimitación de especies; filogenia de cpDNA

The genus Aporocactus Lem. is an epiphytic or saxicolous cactus that is endemic to Mexico and is distributed across the states of Guanajuato, Hidalgo, Puebla, Queretaro, Veracruz, and Oaxaca; these species occupy the canopies of mature trees in cloud forests and Pinus-Quercus forests (Bravo-Hollis 1978, Guzmán et al. 2007). Aporocactus is a very popular cultivated plant in Mexican gardens and is known as the “flor de látigo, floricuerno, junco, rattail cactus” because of its stems. However, as with many members of Cactaceae, Aporocactus exhibits taxonomic issues that have hindered its taxonomic stability. Aporocactus was created by Lemaire (1860) to group species with cylindrical stems that hang more than a metre and zygomorphic pink flowers. Lemaire (1860) included three species in the genus: A. flagelliformis Lem. (= Cactus flagelliformis L.), A. baumannii Lem. (= C. baumannii Lem.), and A. colubrinus (= C. colubrinus Otto ex. C.F. Först.), and this author included C. leptophis D.C. as a synonym of A. flagelliformis. However, A. baumannii and A. colubribus were transferred by Lemaire to the South American genus Cleistocactus Lem., which also presents repent stems and zygomorphic pink flowers. Later, Lemaire (1868) transferred Cereus flagriformis Zucc. ex Pfeiff. to Aporocactus. In the preceding century, Britton & Rose (1920) recognized the genus Aporocactus as delineated by Lemaire (1860, 1861) and accepted five species: A. flagelliformis, A. leptophis (C. leptophisDe Candolle 1829), A. flagriformis, A. martianus (C. martianusZuccarini 1832), and A. conzattii Britton & Rose. Similarly, Bravo-Hollis (1978) recognized the genus Aporocactus and the five referred species. The International Organization for Succulent Plant Study (IOS) drastically reduced this number of species, recognizing Aporocactus as having only two species (Hunt & Taylor 1986). Hunt (1989) argued that “the northern (Hidalgo) species has markedly zygomorphic purplish pink flowers, the southern (Oaxaca) nearly regular scarlet flowers and somewhat stiffer stems'', which correspond to A. flagelliformis and A. martianus, respectively. The other three names were assigned synonyms of the two aforementioned species. The recognition of species in Aporocactus presents a number of problems and a degree of complexity, since all of the existing descriptions were generated based on a few morphological characters (Linneo 1753, Lemaire 1860, De Candolle 1829, Zuccarini 1832, Britton & Rose 1920). However, most of the morphological characters indicated by these authors are continuous, without discrete variation; therefore, it is difficult to recognize the number of species using only morphological characters, with the possible exception of floral symmetry.

Another level of complexity has been the generic position and phylogenetic relationships of this genus. Barthlott (in Taylor & Hunt 1991) included Aporocactus in Disocactus Lindl. as a subgenus because the diurnal magenta and reddish flowers are similar to those exhibited by some species of Disocactus. Barthlott (in Taylor & Hunt 1991), Anderson (2001), Bauer (2003), and Hunt et al. (2006) maintain this criterion under the argument that Disocactus includes all diurnal and colourful flowers, as is also observed in Aporocactus. The studies of Cruz et al. (2016) and Korotkova et al. (2017) have demonstrated that Aporocactus is a monophyletic group that does not belong to Disocactus and that these genera are not directly related. In those phylogenies, the position of Aporocactus inside the tribe Hylocereeae has not been determined. Also, the recent work by Martínez-Quezada et al. (2020) using molecular markers, morphology, and stem anatomical features helped to elucidate the position of Aporocactus. However, the sisterhood with the clade formed by Selenicereus and Weberocereus is supported by the presence of adventitious roots, a character that is present in other genera of the tribe, and the Bayesian analyses using the same dataset did not confirm this relationship.

Aporocactus occupies an atypical ecological niche for cacti. An ecological niche is defined as the set of abiotic and biotic conditions where a species can persist indefinitely (Hutchinson 1957). The fundamental niche of a species is determined by the set of abiotic conditions that defined its physiological range of tolerance in absence of biotic interactions, while the realized niche of a species refers to the space of the fundamental niche where the species actually occurs and limited by biotic interactions (Hutchinson 1957, Soberón & Arroyo-Peña 2017). It is considered that among closely related species, ecological niches have low differentiation, which is a phenomenon known as niche conservatism (Peterson et al. 1999). However, in some empirical studies, niche conservatism is not observed (Ortiz-Medrano et al. 2016), since spatial and temporal climatic variation can influence evolutionary processes. Aporocactus represents a small monophyletic group, and regardless of the number of species, this genus constitutes an interesting taxon to explore the climatic variables that define the niche of each species and inquire whether the niche has been conserved or diverged during speciation. The approaches proposed by Warren et al. (2008) to test whether the observed ecological niche models vary significantly from each other or the from the ‘background’ niche in which they occur have been used to suggest niche conservatism or divergence in some taxa (Pyron et al. 2015). The aim of this research is to conduct a study to delimit the species that conform to Aporocactus, to propose a hypothesis that supports the phylogenetic relationships of the genus in Hylocereeae, and to suggest climate similarity or difference in Aporocactus.

Materials and methods

Plant material and taxon sampling. Plant material of Aporocactus species was collected from wild locations across the states of Hidalgo, Querétaro, Oaxaca, Puebla, and Veracruz in the springs of 2015 and 2016. Sampling included the type localities for the published names (when included in the protologue). For each locality, a section of stem was collected, and a fragment was subsequently herborized and deposited in MEXU; the second fragment was cultivated in the tempered greenhouse in the Botanical Garden of the Institute of Biology at UNAM (JB-IBUNAM), where a tissue sample was obtained, dried and stored in silica gel at -20 °C for subsequent DNA extractions. We included 50 taxa from Hylocereeae as ingroups, 21 of which corresponded to different localities of Aporocactus (Appendix 1), and the remaining 35 taxa corresponded to the genera Acanthocereus (Engelm. ex A. Berger) Britton & Rose, Disocactus Lindl., Epiphyllum Haw., Pseudorhipsalis Britton & Rose, Selenicereus (A. Berger) Britton & Rose, and Weberocereus Britton & Roses from the same tribe. The outgroup consisted of seven species from seven genera pertaining to the sister tribes: Bergerocactus Britton & Rose, Cephalocereus Pfeiff., Stenocereus (A. Berger) Riccob., Echinocereus Engelm., Deamia Britton & Rose, Myrtillocactus Console, Marshallocereus Backeb., and Leptocereus quadricostatus Britton & Rose. Sampled taxa in each analysis are described below.

Isolation, amplification and sequencing of DNA. For the isolation of total genomic DNA, most of the water-storing tissue was removed from the stems before the remaining cortex tissue was dehydrated in silica gel. The dried plant material was homogenized using a mixer mill (Retsch MM200, Haan, Germany) and extracted using the EZ-10 mini-prep kit for plant genomic DNA (Bio Basic, Inc., Ontario, Canada) following the manufacturer's protocol. The incubation time in the lysis buffer was increased to 120 min at 65 °C due to the tissue type. The concentration and purity of DNA (A260/A260 and A260/A230 ratios) were measured using a spectrophotometer (NanoDrop, peqLab, Erlangen, Germany). The original genomic DNA was stored at -20 °C and working dilutions with a standard concentration of 10 ng/μl were prepared for subsequent analysis in PCR assays. PCR amplification was performed for the rpl16 intron (Hernández-Hernández et al. 2011), trnL-trnF intron (Taberlet et al. 1991), psbA-trnH intergenic spacer (Sang et al. 1997, Tate & Simpson 2003) and trnQ-rps16 intergenic spacer (Korotkova et al. 2010, Shaw et al. 2007). The total volume for the standard sample was 25 µl, which consisted of 2.5 µl of 10X buffer, 0.5 µl dNTPs at 200 µM concentration, 1 µl of BSA, 0.75 µl of MgCl2, 0.3 µl F primer, 0.3 µl R primer, 1.25 µl of DNA Platinum Taq Polymerase (Invitrogen™) at 5 U/µl, 0.6 µl of total genomic DNA and 19.025 µl of H2O. The markers that employed internal primers for sequencing were adjusted to a total volume of 50 µl. The PCR programmes used for each marker were as follows: 1) trnQ-rps16, denaturation at 95 °C × 2’, denaturation at 95 °C × 1’, annealing at 55 °C × 1’, extension at 72 °C × 1’, and extension at 72 °C × 7', for 35 cycles. 2) rpl16/trnL-trnF, denaturation at 95 °C × 2’, 94°C × 1’, annealing at 54 °C × 1’, extension at 72 °C × 1’ 30’’, and extension at 72 °C × 7’, for 30 cycles. 3) psbA-trnH, denaturation at 95 °C × 2, denaturation at 95 °C × 30’’, annealing at 55 °C × 1’, extension at 72 °C × 1’, and extension at 72 °C × 10’, for 30 cycles. The sequencing of the molecular markers was performed in the Laboratory of Genomic Sequencing of Biodiversity and Health from the Biology Institute at the National Autonomous University of Mexico (UNAM).

Sequence alignment. The sequences from Aporocactus samples were quality-checked, assembled and edited using Sequencher® v. 4.8 (Gene Codes, Ann Arbor Michigan USA). The sequences for the species of the genera Acanthocereus, Disocactus, Epiphyllum, Pseudorhipsalis, Strophocactus, Bergerocactus, Cephalocereus, Deamia, and Marshallocereus were obtained from the database of the Laboratory of Systematics of Cactaceae from the Botanical Garden/Institute of Biology, UNAM (Arias et al. 2005, Cruz et al. 2016, Sánchez et al. 2014, Hernández-Hernández et al. 2011, Tapia et al. 2017) (Appendix 1). Additionally, we included the rps3-rpl16 and trnK-matK sequences from Korotkova et al. (2017) to complete the matrix (Appendix 1). Individual sequences were cross-checked for possible assembly failures and subsequently stacked and subjected to primary alignment using the software BioEdit (Hall 1999) and the integrated application ClustalW v.1.74 (Thompson et al. 1994). Furthermore, individual marker matrices were realigned and corrected by eye using Mesquite® software v. 3.03 (Maddison & Maddison 2016).

Phylogenetic analyses. A phylogenetic analysis for delimiting species was performed by using four cpDNA markers (psbA-trnH, trnQ-rps16, rpl16, and trnL-F), including 21 samples of Aporocactus and 16 species from eleven genera of Hylocereeae. On the other hand, a phylogenetic analysis for recovered genus relationships used six cpDNA markers and included 35 species from 15 genera. For both analyses, the cpDNA matrix consisted of six markers: psbA-trnH, trnQ-rps16, rpl16, trnL-F, trnk-matk, and rps3-rpl16. The parameters of the Bayesian analyses were identical for both analyses and were performed in MrBayes v. 3.2.1 (Huelsenbeck & Roquist 2001, Ronquist et al. 2012). The General Time Reversible model (GTR+I+G) was selected as the best substitution model using the Bayesian Information Criterion (BIC), as implemented in jModeltest v. 2.0 (Darriba et al. 2014). The analyses consisted of 10 million generations, sampling of parameters and trees every 1,000 generations, and a burning of 25 % of the resulting trees. The convergence of the chains was evaluated visually from the resulting parameter archive of MrBayes using Tracer v. 1.6 (Rambaut et al. 2018).

Ecological niche modeling. We constructed ecological niche models (ENMs) to predict the current distribution of suitable habitat of the recognized species of Aporocactus. Geographic coordinates of occurrence of each species were obtained from field collection, MEXU herbarium specimens, and unambiguous records from Naturalista (www.naturalista.mx). We discarded duplicate records, records with doubtful identity or geographic location and records from cultivated plants. The accessible area (M area, Soberón & Peterson 2005) was defined by the genus range based on the biogeographical provinces proposed by Morrone et al. (2017) and the distribution of pine-oak vegetation and cloud forest associate to those provinces (Rzedowski 1990). Bioclimatic variables were used at an ~1 km2 spatial resolution compiled by Cuervo-Robayo et al. (2014). We masked those climate layers to the extent of the M area. To avoid collinearity, we discarded one of the bioclimatic variables that was highly correlated with another (Spearman correlation values > 0.79) for the study area. Nine variables were used in the final analysis (BIO2, BIO4, BIO10, BIO11, BIO13, BIO14, BIO15, BIO18, and BIO19). For each species, we constructed an ENM using MAXENT v. 3.4.1 (Phillips et al. 2017) through package “dismo” in R v. 4.0.4 (R Core Team 2020). We thinned occurrence points to 1 km2 to avoid spatial autocorrelation. We built different models with 10,000 random background points and evaluated them with spatial-cross validation. We used no campling and different parametrization for Maxent, combining regularization multipliers in intervals of 0.5 ranging from 0.5 to 5, and feature class combinations of Linear, Quadratic, Hinge and Product: L, H, LQ, LH, LQH, and LQHP. We performed the evaluation process with the spatial cross validation procedure “random k-fold” (number of folds = 4) using the R package ENMeval v. 2.0.1 (Kass et al. 2021) with R. Model selection was made based on the Akaike information criteria corrected for small sample sizes (ΔAICc), that reflects a comparison of the goodness-of-fit and parsimonious model (Muscarella et al. 2014). We projected the models using the Maxent “cloglog” transformation. Finally, we evaluated variable importance with Maxent´s variable jackknife test (Phillips et al. 2006). Final models were constructed with ten cross-validation replicates without extrapolation.

Niche identity and similarity. The differences between the niches of the species recognized in Aporocactus were evaluated by using niche overlap, niche identity, and niche similarity analyses in ENMtools (Warren et al. 2010). Niche overlap was calculated through Schoener’s index (D) and Hellinger’s-based I index, which measures the similarity between predictions of habitat suitability (ENM) of one or more pairs of species (Warren et al. 2008, 2010). The niche identity test indicates whether the ENMs produced by two species are identical. The test pools the georeferenced data points for a pair of species, randomizes the taxon identities of these data points, and extracts two new samples with the same sizes as the two original samples. This process is replicated and generates a null distribution of overlap scores, which is compared with the empirical niche overlap scores (Warren et al. 2010). The background similarity test compares the ENM of taxon “A” to an ENM created from n random points drawn from the geographic range of taxon “B”, which generates a null distribution of overlap scores (Warren et al. 2008, 2010). This method is subsequently repeated in the other direction for both taxa in the comparison (B vs. A background). Finally, the test compares the empirical niche overlap of two taxa to a null distribution of overlap scores generated. A total of 100 replicates were run for the niche identity test and background similarity test to assess the differences between the habitat suitability scores defined in the ENMs for both species.

Results

Species delimitation analysis. Four molecular markers were amplified for the ingroup and the outgroup species (Appendix 1). The matrix for the species delimitation analysis was 3,354 bp in length from four concatenated molecular markers (psbA-trnH, rpl16, trnL-F, and trnQ-rps16). Phylogenetic analysis for species delimitation recovered the genus Aporocactus as a monophyletic group (posterior probability (pp) = 1, Figure 1). Two main clades were observed for Aporocactus. One clade included 13 samples from the states of Queretaro, Hidalgo, and Veracruz, which represented the putative taxa A. flagelliformis, A. flagriformis, and A. leptophis. None of those taxa was recovered as a monophyletic group. This clade was well supported (pp = 1) by 11 substitutions: three in psbA-trnH, two in rpl16, and six in trnL-F. The second clade was composed of eight terminals from Oaxaca and Veracruz and included the putative taxa A. martianus and A. conzattii. This second clade was well supported (pp = 1) by four molecular sites: one in rpl16 and three in trnL-F (positions 1,769, 2,000, 2,456). Additionally, the three samples of A. conzattii were recovered in a monophyletic group (pp = 1).

Figure 1 Species delimitation in Aporocactus. Cladogram of the majority rule consensus tree from the Bayesian analysis of the concatenated trnQ-rps16, trnL-trnF, psbA-trnH, and rpl16 markers. Numbers above branches are the Bayesian posterior probability values. 

Phylogenetic relationships analysis. The alignment to infer the phylogenetic relationships of Aporocactus was 6,920 bp in length from six concatenated DNA markers (psbA-trnH, rpl16, trnL-F, trnQ-rps16, trnk-matk, and rps3-rpl16). The analysis to infer the phylogenetic relationships of Aporocactus recovered three principal clades with good support: the hylocereoid clade (pp = 0.9), the phyllocactoid clade (pp = 1), and the Acanthocereus clade (pp = 1) (Figure 2). Aporocactus was resolved as a well-supported monophyletic group (pp = 1) in the hylocereoid clade and was positioned in an early divergent group sister to Selenicereus and Weberocereus (pp = 0.9). In this analysis, the genera Disocactus, Epiphyllum, and Pseudorhipsalis were nested in the phyllocactoid clade, while Acanthocereus was recovered as the earliest diversified lineage in Hylocereeae (Figure 2). The relationship between hylocereoid and phyllocactoid clades in this analysis had low support (pp = 0.7).

Figure 2 Phylogenetic relationships in Aporocactus. Cladogram of the majority rule consensus tree from the Bayesian analysis of the concatenated trnk-matk, rps3-rpl16, trnQ-rps16, trnL-trnF, psbA-trnH, and rpl16 markers. Numbers above branches are the Bayesian posterior probability values. 

Distribution, ecological niche modeling, and niche comparison. Based on Figure 1, the A. flagelliformis clade was determined to be primarily distributed in the Sierra Madre Oriental (Morrone et al. 2017) through Querétaro, Guanajuato, Hidalgo, northern Puebla, and central Veracruz; while the A. martianus clade occupies primarily Sierra Madre del Sur (Morrone et al. 2017) from central Veracruz to southern Puebla and Oaxaca (Figure 3A). The distribution limits of both clades of Aporocactus were observed to converge in central Veracruz state, where Sierra Madre Oriental and Sierra Madre del Sur intersect with the Mexican Transvolcanic Belt (Morrone et al. 2017). Both species were determined to be clearly distributed in pine-oak forests and cloud forests in those biogeographical regions. Accordingly, these clades were recognized as different species: A. flagelliformis and A. martianus. Those clades were determined to be congruent with the current taxonomy of the genus (see discussion).

Figure 3 Actual and potential distribution of Aporocactus. A) Actual distribution of the genus Aporocactus, PdO: Pico de Orizaba, CP: Cofre de Perote, Xa: Xalapa volcanic field, CHPs: Chiconquiaco-Palma Sola. B) ENM of Aporocactus flagelliformis. C) ENM of Aporocactus martianus

Selected ecological niche model (ENM) for A. flagelliformis presented LQ features and regularization multiplier of 0.5 (ΔAIC ≈ 0, Table S1 and Figure S1). The ENM showed the AUC value = 0.947 (S2). Projected ENM of A. flagelliformis added as suitable areas a number of pine-oak and cloud forests in Nuevo León, Tamaulipas, southern Veracruz, and Oaxaca (Figure 3B). The variable with the highest percent contribution in the A. flagelliformis ENM was BIO18 (precipitation of warmest quarter) (24.3 %), followed by BIO14 (precipitation of driest month) (19.3 %), and BIO4 (temperature seasonality) (16.5 %). Variables with the highest permutation importance were BIO4 (36.8 %) and BIO18 (18.6 %). In the case of A. martianus, selected ENM presented LQH features and regularization multiplier of 2 (ΔAIC ≈ 0, Table S2 and Figure S2). This ENM showed an AUC value = 0.928 (S4). Projected ENM of A. martianus added some areas of pine oak forest in northern Puebla and Veracruz and northern Guerrero as suitable areas for the species (Figure 3C). The variables with the highest contribution to the ENM of A. martianus were BIO2 (mean diurnal range) (43 %) and BIO18 (28.8 %). The variable with the highest permutation importance was BIO2 (62.5 %).

Niche analyses indicated that empirical niche overlap between A. flagelliformis and A. martianus was low for de D index (D = 0.261); and moderate for the I index (I = 0.654). The identity test indicated that the ENM between the two species was significantly different (DH0 = 0.772 ± 0.038 vs. DH1 = 0.261 and IH0 = 0.947 ± 0.017 vs. IH1 = 0.654) (Figure 4A). The background similarity test comparing A. flagelliformis ENM in the A. martianus background and vice versa showed that the observed values of empirical niche similarity (D = 0.261, I = 0.654) were lower than expected under the null distribution (Figure 4B, C), indicating that the niches of the two species were significantly different than expected by chance in the available background environments.

Figure 4 Niche conservatism inference in Aporocactus. A) Niche identity test, green bars: D index frequency from null distribution, pink bars: I index frequency from null distribution, green arrow: empirical niche overlap D index, pink arrow: empirical niche overlap I index. B) Niche similarity test of Aporocactus flagelliformis as focus species and A. martianus as background. C) Niche similarity test of Aporocactus martianus as focus species and A. flagelliformis as background. For B) and C), blue bars: D index frequency from null distribution, orange bars: I index frequency from null distribution, blue arrow: empirical niche overlap D index, orange arrow: empirical niche overlap I index. 

Discussion

Species delimitation in Aporocactus. Considering monophyly as a property to recognize species, as well as the geographic distribution and floral morphology of each clade, our results indicated that the two clades in Aporocactus represent two different species (separately evolving metapopulation lineages, De Queiroz 2007). The first clade is formed by the samples initially identified as A. flagelliformis, A. flagriformis, and A. leptophis, but no internal group is formed based on these putative names or by their geographic origin; therefore, in this study, we recognize that samples comprise one species. It is worth mentioning that samples corresponding to the name A. leptophis and A. flagriformis were collected in their respective type localities (Zimapán, probably los Mármoles, Hidalgo and San José del Oro, Hidalgo, respectively). However, those have morphological features corresponding to the variation reported for A. flagelliformis. All samples included in this clade from Querétaro, Hidalgo, and northern Veracruz present zygomorphic flowers and magenta tepals (Figure 5A, B, C, D). Aporocactus flagelliformis (L.) Lem. (≡Cactus flagelliformis L.) is the first published name of the three samples mentioned above, and according to the principle of priority (Art. 11, Turland et al. 2018), it is the correct name for this species. The second clade includes the samples previously identified as A. conzattii and A. martianus (Figure 1). All specimens were distributed from central Veracruz to Oaxaca and exhibited actinomorphic symmetry with red tepals (Figure 5E, F, G, H, I, J). In this case, the name Aporocactus martianus (Zucc.) Britton & Rose (≡Cereus martianus Zucc.) has priority. This result is in keeping with the proposal of Hunt (1989), who discussed the recognition of a northern species with zygomorphic purplish pink flowers and a southern species with regular scarlet flowers, assigning names on base to the ancient name. Hunt (1989) considered A. flagriformis and A. leptophis as stem and flower variations of A. flagelliformis and considered that A. conzattii is a re-description of A. martianus. Notably, a subclade was recovered with the samples of A. conzattii (Figure 1) from the Sierra Madre de Oaxaca at the Sierra Madre del Sur province. However, no particular character was observed in those samples of A. conzattii (Figure 5G), and this group probably represents the population genetic structure of A. martianus. We did not observe any infraspecific entity in A. martianus. Our results agree with the current taxonomy of Aporocactus, which recognizes two species for the genus (see Taxonomic treatment section in Korotkova et al. 2017). Wide variation in flower colour and size was observed, ranging from pink to magenta and from 4 to 7 cm in A. flagelliformis and from light red to deep red and from 7 to 12 cm in A. martianus (Figure 5).

Figure 5 Aporocactus flowers and their variation in color and sizes. A-D) Aporocactus flagelliformis, pink to magenta flowers, all zygomorphic [A, S. Arias 1225, Hidalgo; B, I. Rosas 006, Querétaro; C, I. Rosas 022, Veracruz; D, I. Rosas 024, Hidalgo]. E-J) Aporocactus martianus, light red to deep red flowers, with short to long receptacular tube, actinomorphic [E, M. A. Cruz 09, Oaxaca; F, I. Rosas 17, Oaxaca; G, I. Rosas 14, Oaxaca; H, I. Rosas 15, Oaxaca; I, M. A. Cruz 02, Veracruz; J, I. Rosas 08, Oaxaca]. 

Phylogenetic relationships of Aporocactus. The results supported the monophyly of the genus Aporocactus (Cruz et al. 2016, Korotkova et al. 2017) and rejected the hypothesis of some authors that Aporocactus is a member of Disocactus because of the similarity in the shape, colour, and diurnal anthesis of these plants, which are presumably pollinated by hummingbirds (Barthlott in Taylor & Hunt 1991, Bauer 2003, Hunt et al. 2006). These results indicated that Aporocactus and Disocactus are independent lineages in different clades and suggest that diurnal anthesis in bright-coloured flowers appeared independently at least two times in Hylocereeae. In the sister tribe Echinocereeae, hummingbird pollination syndrome independently evolved in Morangaya pensilis (K. Brandegee) G.D. Rowley, Echinocereus section Triglochidiati Bravo, Stenocereus alamosensis (J.M. Coult.) A.C. Gibson & K.E. Horak and S. kerberi (K. Schum.) A.C. Gibson & K.E. Horak (Sánchez et al. 2014). Martínez-Quezada et al. (2020) postulated that Aporocactus has two anatomical synapomorphies in the stem: 1) a delay in fibre development in the wood and 2) cortical bundles with secondary growth. In field work, we observed that Aporocactus plants do not develop wood, as occurs in other genera, such as Disocactus or Selenicereus; instead, in the base of the oldest stem in Aporocactus, the roots release them and promote vegetative propagation.

Aporocactus was recovered as a sister to Selenicereus + Weberocereus in the hylocereoid clade. This result was significant, since Korotkova et al. (2017) did not recover these relationships by using cpDNA markers only. We noted that the addition of cpDNA markers in the present study results in a more resolved phylogeny. This sisterhood (Aporocactus (Selenicereus and Weberocereus)) was also achieved by Martínez-Quezada et al. (2020) by using the cpDNA markers from Korotkova et al. (2017) and a complement of morpho-anatomical characters. Martínez-Quezada et al. (2020) suggest that the hemiepiphytic condition and the presence of adventitious roots along the stem represent the synapomorphies of this clade. Nevertheless, other members of Hylocereeae, such as Disocactus and Epiphyllum (phyllocactoid clade), can develop this type of root frequently in different stages of growth (juvenile, adult); rather, this root represents a homoplasy, which in combination with other characters is useful to diagnose the hylocereoid clade. It is important to highlight that in the absence of more DNA sequences, the addition of morphological characters can be useful for obtaining a more resolved topology, as observed in other cacti (Sánchez et al. 2018, Vargas-Luna et al. 2018, Martínez-Quezada et al. 2020).

Distribution of Aporocactus. The known distribution of Aporocactus (Figure 3A) was restricted to the old pine-oak and cloud forests. As suggested by Hunt (1989), A. flagelliformis represents the northern species through the Sierra Madre Oriental and extends to central Veracruz in the Transmexican Volcanic Belt. Traditionally, the distribution of A. martianus was only reported in Oaxaca at the Sierra Madre del Sur; however, our results showed that this species is also distributed in central Veracruz, at the limit of the Transmexican Volcanic Belt. Although the distribution of both species converges in central Veracruz, a detailed analysis of this region indicated that A. flagelliformis and A. martianus present an allopatric distribution. Our results suggested that speciation of the ancestral Aporocactus lineage was influenced by the formation of the modern Transmexican Volcanic Belt in the eastern part during the late Pliocene-Quaternary (2.0-0.1 ma) (Rodríguez et al. 2010). A similar biogeographic pattern is also observed in other epiphytic sister species, namely, Disocactus phyllanthoides and D. ackermannii (Cruz et al. 2016). Even the vicariant consequence of the Transmexican Volcanic Belt can be observed in sister species, such as Cephalocereus senilis and C. columna-trajani (Tapia et al. 2017), in the lower western parts of the Sierra Madre Oriental and Sierra Madre del Sur.

Niche modeling and niche conservatism. Temperature and precipitation are the main factors determining the altitudinal and longitudinal plant distribution (Archibold 1995). It has been proposed that precipitation and humidity variations have a more prominent effect on epiphytic plants (Hernández-Ruíz et al. 2016, Zotz 2016). Even in the globular cactus Thelocactus, precipitation (precipitation in the wettest quarter) constrains the ENM for most species (Mosco 2017). This pattern coincides for the ENM of Aporocactus flagelliformis, in which precipitation of the warmest month (BIO18) and the driest month (BIO14), and the temperature seasonality defined the model. Also, for A. martianus, the mean diurnal range (BIO2) and precipitation of the warmest month (BIO18) defined the model. Temperature seasonality is considered important in growth and other phenological processes (Menzel & Sparks 2006). The latter factor is critical for the conservation of Aporocactus and other epiphytic cacti in the context of climate warming. Although other regions with high suitability of distribution for A. flagelliformis were recovered, it is necessary to corroborate their presence in particular zones (e.g., Sierra Madre Oriental at San Luis Potosí) or to investigate biological factors limiting the actual distribution (e.g., pollinator availability).

Analyses suggested that the niche overlap is low and niches of the two species of Aporocactus are not identical and are significantly differentiated. Species of Aporocactus have specific environmental constraints and do not occupy niches that are similar as possible given what is available. Epiphytic plants in cloud forests are especially sensitive to climate changes (Foster 2001), floristic and climatic differences have been documented for cloud forests in Hidalgo, Querétaro, and central Veracruz versus cloud forests in southern Veracruz and Oaxaca (Ruíz-Jiménez et al. 2012). Comparative analysis of niche overlap and niche similarity has been addressed in other close related Mexican plants and cacti, and lead some authors to consider the existence of niche conservatism on those lineages (Suárez-Mota et al. 2015, Mosco 2017, Gutiérrez-Ortega et al. 2020), however our results suggest niche divergence in these sister species. A critical review by Münkemüller et al. (2015) suggests that studies investigating niche conservatism should compare alternative evolutionary models, including multiple-optima OU models. A comparative niche evolution analysis, as previous authors recommend, including a wider sampling of the tribe Hylocereeae, will allow to corroborate phylogenetic niche conservatism and niche shift in the Mesoamerican epiphytic lineages of cacti. For now, base on the difference of the ecological niches, we suggest the possibility of niche divergence in Aporocactus, as is expected for allopatric species (Peterson et al. 1999, Warren et al. 2008). Finally, the primary differences between both species of Aporocactus are established by the floral morphology; therefore, it is likely that the primary factor driving the evolution of these lineages is their association with pollinators. For many years, epiphytic cactus species have received scarce attention. Although Aporocactus is a small genus, it may represent an interesting model for research on such topics as the ecology of pollination, population genetics, and flower development to characterize the evolution of those specialized cacti.

Supplementary material

Supplemental data for this article can be accessed here: https://doi.org/10.17129/botsci.2893

Supplementary material Figure S1, Figure S2, Table S1 and Table S2.

Acknowledgements

SA thanks the DGAPA/PAPIIT IN208619 project for funding this project. IRR thanks Programa de Posgrado en Ciencias Biológicas de la Universidad Nacional Autónoma de México (UNAM) and CONACyT for the master scholarship (CVU No. 631277). DS thanks the programme Investigadoras e investigadores por México CONACYT (project 985). We thank A. García for the figure design and photo editing shown in Figures 1, 2 and 3. Additionally, thanks are due to C. Cervantes and D. Franco for assisting with field collections and to Y. Morales for providing support with living collections. We thank S. Estrada-Marquez for comments and discussion on ecological niche modelling. We are especially grateful to the anonymous reviewers and associate editor for their comments to improve the manuscript.

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Appendix 1.

Taxa included in plastid rpl16, trnL-F, psbA-trnH, trnQ-rps16, trnk-matK and rps3-rpl16 phylogenetic analyses. The sequences lacking for a locus/specimen GenBank accession are marked with dash (-), N.A.: no data 

Taxon Source, Voucher GenBank accession number
rpl16 trnL-F psbA-trnH trnQ-rps16 trnk-matk rps3-rpl16
Acanthocereus chiapensis Bravo MX: Chiapas, Guzmán 999, MEXU KU598005 KU598057 KU597952 KU598110 HM041754.1 _
Acanthocereus oaxacensis (Britton & Rose) Lodé MX: Oaxaca, Arias 2185, MEXU KU598008 KU598060 KU597955 KU598113 _ _
Acanthocereus tetragonus (L.) Hummelinck MX: Chiapas, Guzmán 1002, MEXU KU598021 KU598074 KU597969 KU598127 HM041645.1 _
Aporocactus flagelliformis (L) Lem. MX: Hidalgo, Rosas 01, MEXU MZ836110 MZ836080 MZ836172 MZ836141 LT745632 LT745515.1
Aporocactus flagelliformis (L) Lem. MX: Hidalgo, Rosas 02, MEXU MZ836118 MZ836081 MZ836181 MZ836150
Aporocactus flagelliformis (L) Lem. MX: Hidalgo, Rosas 04, MEXU MZ836119 MZ836082 MZ836182
Aporocactus flagelliformis (L) Lem. MX: Hidalgo, Rosas 023, MEXU MZ836112 MZ836084 MZ836174 MZ836143
Aporocactus flagelliformis (L) Lem. MX: Hidalgo, Rosas 025, MEXU MZ836113 MZ836175 MZ836144
Aporocactus flagelliformis (L) Lem. MX: Hidalgo, I Rosas 027, MEXU MZ836114 MZ836085 MZ836176 MZ836145
Aporocactus flagelliformis (L) Lem. MX: Hidalgo, I Rosas 029, MEXU MZ836115 MZ836086 MZ836177 MZ836146
Aporocactus flagelliformis (L) Lem. MX: Hidalgo, S. Arias 1221, MEXU MZ836120 MZ836090 MZ836183 MZ836151
Aporocactus flagelliformis (L) Lem. MX: Querétaro, I Rosas 031, MEXU MZ836116 MZ836087 MZ836178 MZ836147
Aporocactus flagelliformis (L) Lem. MX: Querétaro, I Rosas 032, MEXU MZ836127 MZ836088 MZ836179 MZ836148
Aporocactus flagelliformis (L) Lem. MX: Querétaro, I Rosas 033, MEXU MZ836117 MZ836089 MZ836180 MZ836149
Aporocactus flagelliformis (L) Lem. MX: Veracruz, I Rosas 020, MEXU MZ836111 MZ836083 MZ836173 MZ836142
Aporocactus martianus (Zucc.) Britton & Rose MX: Oaxaca, I Rosas 07, MEXU. MZ836121 MZ836091 MZ836184 MZ836152 LT745634 LT745517.1
Aporocactus martianus (Zucc.) Britton & Rose MX: Oaxaca, I Rosas 010, MEXU MZ836122 MZ836092 MZ836185 MZ836153
Aporocactus martianus (Zucc.) Britton & Rose MX: Oaxaca, I Rosas 013, MEXU MZ836123 MZ836096 MZ836186 MZ836154
Aporocactus martianus (Zucc.) Britton & Rose MX: Oaxaca, S. Arias 1225, MEXU MZ836124 MZ836093 MZ836187 MZ836155
Aporocactus martianus (Zucc.) Britton & Rose MX: Oaxaca, Arias 1230, MEXU MZ836125 MZ836094 MZ836188 MZ836156
Aporocactus martianus (Zucc.) Britton & Rose MX: Oaxaca, Arias 2207, MEXU. MZ836126 MZ836095 MZ836189 MZ836157
Aporocactus martianus (Zucc.) Britton & Rose MX: Oaxaca, Cruz 02, MEXU KU597983 KU598035 KU597930 KU598088 _ _
Aporocactus martianus (Zucc.) Britton & Rose MX: Oaxaca, Cruz 09, MEXU KU597986 KU598038 KU597933 KU598091 _ _
Aporocactus martianus (Zucc.) Britton & Rose MX: Oaxaca, Cruz 13, MEXU KU597989 KU598041 KU597936 KU598094 _ _
Aporocactus martianus (Zucc.) Britton & Rose MX: Veracruz, Cruz 01, MEXU KU597980 KU598032 KU597927 KU598085 _ _
Bergerocactus emoryi (Engelm.) Britton & Rose MX: Baja Cal., Arias 1307, CHAPA DQ099994 DQ099925 KF783478 KF783697 HM041654.1 _
Cephalocereus scoparius (Poselg.) Britton & Rose MX: Oaxaca, Hamman N.A. (cult.) AY181596 AY181625 KY624675 KY624747 _ _
Disocactus biformis (Lindl.) Lindl. GT: Sacatepéquez, Véliz 19901, BIGU KU598016 KU598069 KU597964 KU598122 LT745639 _
Deamia chontalensis (Alexander) Doweld MX: Oaxaca, Yañez 03, MEXU MH107788 MH107803 MH107793 LT745733 _
Disocactus phyllanthoides (DC.) Barthlott MX: Veracruz, Arias 2201, MEXU KU598025 KU598078 KU597973 KU598131 LT745651 LT745535.1
Disocactus speciosus (Cav.) Barthlott MX: Jalisco, Morales 01, MEXU KU597992 KU598044 KU597939 KU598097 LT745654 LT745538.1
Echinocereus pentalophus (DC.) Lem. MX: Querétaro, Arias 1737, MEXU KF783558 KF783628 KF783509 KF783699 KF783558.1 _
Deamia testudo (Karw. ex Zucc.) Britton & Rose MX: Oaxaca, Yáñez 001, MEXU KY624648 KY624662 KY624695 KY624765 LT745735
Epiphyllum phyllanthus (L.) Haw. SR: Hammel 22377, INB KU598015 KU598068 KU597963 KU598121 LT745667 LT745550.1
Epiphyllum thomasianum (K.Schum.) Britton & Rose PA: Cocle, Hammel 22020, INB KU598018 KU598071 KU597966 KU598124 LT745672 LT745556.1
Leptocereus quadricostatus Britton & Rose PR: Cabo Rojo, Arias 1464, MEXU KF783620 KF783690 AY851582 KF783768 _ _
Myrtillocactus eichlamii Britton & Rose MX: Yucatan, Arias 1363, MEXU. AY181610 AY181629 KY624690 KY624760 _ _
Myrtillocactus geometrizans Console. MX: Querétaro, Terrazas 557, CHAPA DQ100012 DQ099943 KY624694 KY624764 _ _
Pseudorhipsalis amazonica (Rol.-Goss.) Britton & Rose. PA: Colon, Hammel 24524, INB KU597994 KU598046 KU597941 KU598099 LT745699 LT745582.1
Pseudorhipsalis himantoclada (Rol.-Goss.) Britton & Rose CR: San José, Hammel 22076, INB KU597998 KU598050 KU597945 KU598103 LT745703 LT745586.1
Selenicereus atropilosus Kimnach MX: Jalisco, Arreola 1473, MEXU. KU598029 KU598082 KU597977 KU598135 LT745709 LT745592.1
Selenicereus calcaratus (F.A.C. Weber) D.R. Hunt CR: San José, Hammel 18394, INB MZ836128 MZ836097 MZ836190 MZ836158 LT745674 LT745558.1
Selenicereus dorschianus Bauer MX: Jalisco, Arias 2218, MEXU MZ836129 MZ836098 MZ836191 MZ836159 LT745712 LT745595.1
Selenicereus escuintlensis (Kimnach) D.R. Hunt GT: Escuintla, Véliz 20047 MZ836130 MZ836099 MZ836192 MZ836160
Selenicereus glaber (Eichlam) S.Arias & N.Korotkova MX: Chiapas, Bravo 5614, MEXU KU598031 KU598084 KU597979 KU598137 LT745738 LT745621.1
Selenicereus grandiflorus (L.) Britton & Rose MX: Veracruz, Guzmán 1365, MEXU DQ100039 DQ099970 KU597971 KU598129 LT745713 LT745596.1
Selenicereus guatemalensis (Eichlam ex Weing.) D.R.Hunt. GT: Guatemala, Arias 1161, MEXU MZ836131 MZ836193 MZ836161
Selenicereus inermis (Otto ex Pfeif.) Britton & Rose CR: Puntarenas, Hammel 24274, INB MZ836132 MZ836100 MZ836194 MZ836162 LT745721 LT745604.1
Selenicereus monacanthus (Lem.) D.R.Hunt CR: Heredia, Hammel 26600, INB MZ836133 MZ836101 MZ836195 MZ836163 LT745682 LT745566.1
Selenicereus ocamponis (Salm-Dyck) D.R.Hunt MX: Guerrero, Gama 104, MEXU MZ836134 MZ836102 MZ836196 MZ836164 LT745688 LT745572.1
Selenicereus purpusii (Weing.) S.Arias & N.Korotkova MX: Oaxaca, Guzmán 1095, MEXU MZ836135 MZ836103 MZ836197 MZ836165
Selenicereus stenopterus (F.A.C.Weber) D.R.Hunt CR: Heredia, Hammel 22282, INB MZ836136 MZ836104 MZ836198 MZ836166 LT745729 LT745577.1
Selenicereus vagans (K.Brandegee) Britton & Rose MX: Sinaloa, Arias 1832, MEXU MZ836137 MZ836105 MZ836199 MZ836167 LT745730 LT745614.1
Stenocereus pruinosus (Otto ec. Pffeif.) Buxb. MX:Puebla, Arias 750, MEXU KF783618 KF783688 KF783554 KF783765 _ _
Weberocereus frohningiorum Bauer CR: San José, Hammel 22419, INB MZ836138 MZ836106 MZ836200 MZ836168 LT745737 LT745620.1
Weberocereus imitans (Kimnach & Hutchison) Buxb. CR: San José, Hammel 26140, INB MZ836139 MZ836107 MZ836201 MZ836169 LT745740 LT745623.1
Weberocereus tunilla subsp. biolelly (F.A.C. Weber) Bauer CR: Alajuela, Hammel 25603, INB MZ836140 MZ836108 MZ836202 MZ836170 LT745746 LT745629.1
Weberocereus tunilla subsp. tunilla (F.A.C. Weber) Britton & Rose. CR: Cartago, Hammel 22442, INB MZ836109 MZ836203 MZ836171 LT745745 LT745628.1

Received: June 22, 2021; Accepted: December 01, 2021; Published: January 20, 2022

*Author for correspondence: sarias@ib.unam.mx

Associate editor: Monserrat Vázquez Sánchez

Author Contributions: IRR and SA designed the study. IRR and SA collected the field samples. IRR performed the DNA extractions. IRR and DS performed the phylogenetic analyses and performed the biogeographic analyses. DS performed the ecological niche modeling analyses. IRR and DS wrote the first draft of the manuscript, and SA revised and critically evaluated the manuscript. All the authors approved the final version of the manuscript.

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