Next Article in Journal
Free-Living and Particle-Associated Microbial Communities of Lake Baikal Differ by Season and Nutrient Intake
Previous Article in Journal
Health Status of Stranded Common Bottlenose Dolphins (Tursiops truncatus) and Contamination by Immunotoxic Pollutants: A Threat to the Pelagos Sanctuary—Western Mediterranean Sea
Previous Article in Special Issue
Floral Specialization and Bat Pollination in Subtribe Cereinae (Cactaceae): A Morphological Approach
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Diversity
Volume 15
Issue 4
10.3390/d15040570
diversity-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Phylogenomics of One of the World’s Most Intriguing Groups of CAM Plants, the Opuntioids (Opuntioideae: Cactaceae): Adaptation to Tropical Dry Forests Helped Drive Prominent Morphological Features in the Clade

by
Lucas C. Majure
1,2,*,
Serena Achá
1,
Marc A. Baker
3,
Raul Puente-Martínez
2,
Matias Köhler
4 and
Shannon Fehlberg
2
1
Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA
2
Department of Research, Conservation and Collections, Desert Botanical Garden, Phoenix, AZ 85008, USA
3
College of Liberal Arts & Sciences, Arizona State University, Tempe, AZ 85287, USA
4
Programa de Pós-Graduação em Botânica, Universidade Federal do Rio Grande do Sul, Porto Alegre 91501970, RS, Brazil
*
Author to whom correspondence should be addressed.
Diversity 2023, 15(4), 570; https://doi.org/10.3390/d15040570
Submission received: 3 March 2023 / Revised: 14 April 2023 / Accepted: 16 April 2023 / Published: 18 April 2023
(This article belongs to the Special Issue Anatomy, Ecology and Evolution of Cactaceae)
Browse Figures
Versions Notes

Abstract

:
Opuntioideae, composed of roughly 370 species, occur in almost every biome in the Americas, from seasonally dry tropical forests (SDTF) to high-elevation Andean grasslands, American deserts and temperate zones. The interrelationships among the three major clades of Opuntioideae (Cylindropuntieae, Opuntieae and Tephrocacteae) are not well resolved, and thus, the ancestral habitat, biogeographic history and evolution of morphological characters, such as large photosynthetic leaves and flattened stems, are poorly understood. To test their geographic origin and evolution of key morphological characters, we built the largest phylogenomic dataset for Cactaceae to date using 103 plastid genes of 107 taxa of Opuntioideae. The subfamily Opuntioideae likely evolved in South America in a combination of seasonally dry tropical forest (SDTF)/desert habitats. Opuntieae most likely evolved in South America in SDTF and, from there, moved into desert regions, Chaco and temperate/subtropical zones, while Tephrocacteae and Cylindropuntieae evolved in South America in desert regions and moved into SDTF, Chaco and temperate/subtropical zones. Analyses of morphological evolution suggest that, although large leaves are plesiomorphic in Opuntioideae, long-lived, photosynthetically active leaves in Cylindropuntieae and Tephrocacteae are homoplasious and do not represent retained plesiomorphy, as is often assumed. Flattened stems are synapomorphic for Opuntieae, possibly representing adaptation to competition for light resources in SDTF, their most likely ancestral area.

1. Introduction

The Cactaceae clade (Caryophyllales, Portulacineae) is an endemic New World group of mostly stem succulents that occur in arid and semi-arid, or at least edaphically arid, areas throughout the Americas [1,2,3] (although see Rhipsalis baccifera (Sol.) Stearn [4,5,6,7,8,9,10]). Most recent phylogenetic studies show Cactaceae to be most closely related to Portulacaceae s.s., i.e., Portulaca L. [11,12,13,14,15,16] or Anacampserotaceae [17], or as sister to a Portulacaceae + Anacampserotaceae clade [18,19,20,21]. Putative ages for the clade have been proposed based on rates of the molecular evolution of ITS [22], as well as calibrated phylogenies based on fossil constraints outside of Cactaceae [23,24], given that no macrofossils beyond the Pleistocene are known from the clade. All three estimates suggest an Oligocene origin for the crown clade of Cactaceae (ca. 30 Ma, although see [11] for a younger putative age or [25] and [15] for older ages). However, most of the diversity within the group is estimated to have arisen during the mid-Miocene and later, in concert with reduced CO2 levels and increased aridification across the Americas [23].
The leafy members of Cactaceae, Leuenbergeria and Pereskia (i.e., “Pereskia s.l.”), have most recently been resolved as subsequent sisters to the rest of the more derived, mostly stem photosynthetic cacti [18,20,26,27]. Maihuenia (sometimes placed in Maihuenioideae [28]), a C3 taxon with large, persistent, cylindrical leaves, has been recovered as sister to the major clade Cactoideae [18,19,20,26,29] or as sister to the Cactoideae + Opuntioideae clade or in other positions [30]. Cactoideae and Opuntioideae are the most diverse groups in the family, with 1000+ and ca. 370 species, respectively [3], and have been recovered as monophyletic in numerous analyses [11,23,26,29,30,31,32,33,34,35].
The bulk of phylogenetic work in Cactaceae has been focused on smaller groups within the most diverse subfamily Cactoideae [36,37,38,39,40,41,42,43,44,45,46,47,48,49,50]. However, renewed interest has also developed for Opuntioideae [51,52], a group that was once placed mostly under a single genus, Opuntia (L.) Mill. s.l. [1]. In the past 20 years, numerous phylogenetic studies have focused on Opuntioideae [29,32,35,53,54], including phylogenetic studies of the well-supported tribes Opuntieae DC. (prickly pear cacti and relatives; see [55,56,57,58]), Tephrocacteae Doweld (Andean Opuntias and relatives; see [59,60]) and Cylindropuntieae Doweld, the chollas and relatives [29,53,61].
Phylogenetic relationships among the three tribes are contentious, with some analyses reporting Opuntieae as sister to a Tephrocacteae + Cylindropuntieae clade [29], while other analyses show Cylindropuntieae as sister to an Opuntieae + Tephrocacteae clade [20]. Plastid data have shown the former, while nuclear data have sometimes shown the latter. However, Kohler et al. [35] also showed that different combinations of plastid genes could resolve either relationship. Thus, this is a pattern deserving further study. Previous results have shown that both Opuntieae and Cylindropuntieae likely originated in South America and then subsequently dispersed into North American drylands and elsewhere, where they radiated substantially [29,55]. However, it is still unclear what habitats those two tribes may have evolved in. Likewise, the geographic origin of the mostly Andean Tephrocacteae is as yet unexplored.
Cactoideae are considered to be the most derived members of the caulocacti with extremely reduced or microscopic (vegetative plant body) photosynthetic leaves [62,63], while the Opuntioideae apparently exhibit retained ancestral characters, such as relatively large (macroscopic) leaves of the vegetative plant body [29]. However, two members of the Opuntioids, Quiabentia from the South American Chaco and Brazilian Caatinga and Pereskiopsis from Central American and Mexican seasonally dry tropical forests (SDTF), have very large, flattened leaf blades, very similar to those of Leuenbergeria and Pereskia. Likewise, certain species of Austrocylindropuntia, mostly from Andean SDTF or scrub vegetation, produce large, persistent leaves. These leafy taxa have also been reported to exhibit facultative CAM [11,64], a character state reported for other members of Opuntioideae, including Opuntia [64,65], as opposed to obligate CAM in most other, more derived Cactaceae [64]. Although often considered to be a retained plesiomorphy [64,66], Majure et al. [29] suggested that the photosynthetically functional leaves of Quiabentia and Pereskiopsis were actually derived secondarily after the drastic reduction in leaf size in most Opuntioids (in concert with increased stem photosynthesis); however, their taxon sampling within Opuntioideae, as well as of outgroup taxa, was greatly limited.
Another key feature in the Opuntioids, specifically the tribe Opuntieae, is the production of flattened stems. This is a morphological feature that is apparently restricted to Opuntieae within the Opuntioids, although other cacti outside of the subfamily have also developed similar flattened stem segments, such as Epiphyllum, which grows epiphytically in low-light situations. Interestingly, Brasiliopuntia and Consolea, which oftentimes grow in dense SDTF, produce these flattened stem segments, which are relatively thin and somewhat ephemeral, effectively acting as leaves. It is also curious that species of Opuntia occurring in more xeric and high-light conditions often produce copious areoles and spines and/or a pubescent epidermis (Majure, unpubl. data). Thus, there appear to be morphological characters that are directly affected by and perhaps correlated with specific environments, but these morphological features have not been analyzed in a phylogenetic framework.
Here, we expanded on previous phylogenetic analyses with increased sampling in the subfamily Opuntioideae (107 taxa) to test the relationships among the three major Opuntioid clades. We also broadly sampled all major clades in Cactoideae (47 taxa) to test the resolving power of our plastome dataset, as well as “leafy” outgroup taxa, such as Leuenbergeria, Maihuenia, Pereskia, Aizoaceae, Anacampserotaceae, Didiereaceae, Molluginaceae, Montiaceae and Portulacaceae, to revisit the evolution of large photosynthetic leaves in Opuntioideae, as well as other key morphological characters, such as the curiously flattened stems of Opuntieae. We used our phylogeny to determine the putative ancestral habitat, divergence time estimation and geographic origin of the Opuntioid clade.

2. Materials and Methods

2.1. Taxon Sampling, DNA Extraction and Sequencing

We sampled broadly across Opuntioideae (107 taxa), incorporating representatives from all major clades of the tribes Cylindropuntieae [29], Opuntieae [55] and Tephrocacteae [59,60]. Our sampling of Cylindropuntieae and Opuntieae was mostly restricted to diploid taxa, based on what we know about ploidy in those clades [67,68]. We also sampled all major clades of the subfamily Cactoideae (47 taxa) based on the topology recovered by Hernández-Hernández et al. [30], as well as both clades of “Pereskia” s.l. [26], i.e., Leuenbergeria and Pereskia s.s. These taxa were either field-collected or sampled directly from herbarium specimens or from the living collections at Desert Botanical Garden (https://www.dbg.org/research-conservation/living-collections/; accessed 17 August 2021). Data for Maihuenia, as well as several other cacti [23], were downloaded from GenBank (https://www.ncbi.nlm.nih.gov/genbank/; accessed 17 August 2021), as were raw reads from baited experiments [18], transcriptome sequencing [20] or whole plastome data [69] for Aizoaceae (Mesembryanthemum, Tetragonia), Anacampserotaceae (Anacampseros, Talinopsis), Basellaceae (Anredera), Didiereaceae (Didiera, Portulacaria), Molluginaceae (Mollugo), Montiaceae (Calandrinia, Cistanthe) and Portulacaceae (Portulaca oleracea) (see Section S1).
Each new taxon sampled here was sequenced using genome skimming based on the methods of Majure et al. [29,49,50]. Briefly, whole genomic DNA was extracted from epidermal, root or tepal tissue, which was homogenized in a mortar and pestle or a tissue homogenizer, such as a bead-beater, and a modified CTAB buffer and direct column cleaning were used in silica columns [29,70]. DNAs were sent to Rapid Genomics for library preparation and sequencing on an Illumina HiSeq X platform using paired-end (150 bp) reads.
All raw reads newly generated here, and any reads downloaded from GenBank (plastome or transcriptome or from baited capture methods), were referenced-mapped to the chloroplast genome of Cylindropuntia bigelovii [29] and annotated in Geneious (v. 11.1.5, Biomatters Ltd., Auckland, New Zealand) using our C. bigelovii plastome. All genes (coding, rRNA and tRNA; n = 103) were subsequently extracted in Geneious from the referenced-mapped raw reads and used for alignment. Alignments were carried out with Mafft [71] and then checked manually. Any genes with ≥50% missing data and/or apparent pseudogenes (e.g., accD, ycf1 and ycf2; see [29,35]) were removed from the alignment.

2.2. Phylogenetic Analyses and Divergence Time Estimation

Our plastome gene dataset was analyzed using maximum likelihood in Geneious with the RAxML V. 8.0 plugin [72] using the GTR+Γ model of molecular evolution and undertaking 1000 bootstrap pseudoreplicates. We then used BEAST v2.6.2 [73] to estimate divergence times across Cactaceae. In our BEAST analysis, we searched for optimal partitions in the assembly using the annotated Cylindropuntia bigelovii genome [29] and PartitionFinder2 [74]. Furthermore, we tested the unpartitioned assembly for 88 substitution models using jModeltest 2.1 [75] on CIPRES [76]. We then used treePL v. 1 [77], the RAxML phylogenetic topology and a secondary calibration for the crown age of Cactaceae (28.6 Ma), Cactoideae (24.4) and Opuntieae (25.3) based on ages given in Arakaki et al. [23] to date our phylogeny. We used our treePL chronogram as a starting tree for our analysis in BEAUti and BEAST v2.6.2 [73] on the University of Florida’s high-performance computing cluster (HiPerGator). We applied a Gamma site model using the TPM1uf+I+G model, as supported by jModeltest with a relaxed log-normal molecular clock with a Yule speciation model. After preliminary analyses, the birthrate and ucldMean (uncorrelated log-normally distributed) priors had to be enforced with soft limits (−∞,1 × 10−4), because they failed to reach convergence. Additionally, we provided a secondary calibration for the crown age (28.6 Ma) of Cactaceae [23], and we parameterized it with a normal distribution, enforcing monophyly for the family. Lastly, we performed two independent runs of 100 million generations each, sampling every 10,000 generations. The output logs of these analyses were combined with LogCombiner 2.6.2 [78] and inspected in TRACER 1.7.1, discarding the first 10% percent of the generations. The maximum credibility chronogram was produced using TreeAnnotator v2.6.2 [79], using the mean node height values. Finally, we used Figtree v1.4.2. to visualize the resulting chronogram [80].

2.3. Morphological Evolution across Cactaceae

We reconstructed the evolutionary history of several important morphological characters across cacti, including (A) stem shape, (B) leaf size, (C) leaf shape, (D) leaf duration, (E) growth form, (F) growth type and (G) areole number (only in Opuntieae). Stems were coded as either cylindrical or flattened in cross-section. The leaf size of the vegetative stems was coded as either large (macroscopic) or small (microscopic or totally reduced); it should be noted that some Cactoideae produce large leaves on the reproductive parts of the plant [81], which were not considered in our coding here. Leaf shape was coded as flattened (bifacial) or cylindrical (unifacial), and leaf duration was coded as either ephemeral (caducous after the development of the stem) or long-lasting (i.e., retained even after stem development). The growth form was coded as herb, tree, shrub, and liana or lianescent shrub. The growth type was recorded as either monopodial or sympodial, and the areole number for the tribe Opuntieae was coded as having <30 areoles per cladode face or >30 areoles per cladode face based on data compiled by Majure (unpubl. data). We reconstructed the evolution of morphological characters in Mesquite [82] using maximum likelihood (ML) under the Mk1 model of evolution, which allows for an equally probable rate of change from one state to another, or under maximum parsimony (MP) for characters with polymorphic states.

2.4. Ancestral Range Reconstruction

Using our maximum clade credibility chronogram generated in BEAST, we conducted two ancestral range reconstruction analyses in RASP v4.0 [83] and the R package Biogeobears [84,85,86,87], including the Biogeographical Stochastic Mapping (BSM) component [88,89] on Hipergator (https://www.rc.ufl.edu/services/hipergator/; accessed 4 Mar 2021). First, we designated the ranges based on habitat: (A) seasonally dry tropical forest, (B) desert, (C) temperate/subtropical forest, (D) Chaco and (E) ruderal. Second, we used the ecoregion level 1 units of Griffith et al. [90], in part, based on the distributions of taxa sampled in our phylogeny: (A) Old World, (B) western North American deserts (unit 10), (C) Mexico–Central American tropical dry forests (units 12, 13 and 14), (D) eastern temperate forests and temperate sierras (units 8 and 13), (E) West Indies (unit 16), (F) Chaco (unit 22), (G) Northern, Central and Southern Andes (units, 17, 18 and 19), (H) Eastern Highlands (Brazil—Caatinga) (unit 21) and (I) Pampas (unit 23). We applied the six-model likelihood-ratio test to both analyses: DEC [91,92], DEC+J [86], DIVALIKE [86,93], DIVALIKE+J, BAYAREALIKE [86,94] and BAYAREALIKE+J [86]. We then selected the best model based on the Akaike information criterion (AIC) values [95] and ran a non-stratified ancestral range reconstruction, allowing a maximum of 3 areas per node for the habitat-based reconstruction and 5 for the ecoregion-based reconstruction. We recognize the controversy surrounding the use of the J parameter in model selection [96]; however, given that most of our taxa occupy single areas, the J parameter is appropriate [97].

3. Results

Our PartitionFinder analysis found support for eight partitions; however, none of these partitions produced significantly different phylogenetic trees (PartitionFinder and corresponding RAxML results not shown) when compared to the concatenated tree. jModeltest recovered the model TPM1uf+I+G as the most optimal for the concatenated assembly used in our BEAST analysis.

3.1. Phylogeny and Divergence Time Estimation

Our BEAST (BI) and RAxML (ML) phylogenetic reconstructions recovered a well-supported phylogeny, with most nodes showing 0.95 posterior probability (PP) or 100% bootstrap (bs) support (Figure 1) or higher unless stated otherwise (Supplementary Figure S1). Our divergence time estimation analysis showed very high ESS values (>500) for most parameters, except tree prior (ESS = 38), TreeHeight (ESS = 12), ucldStdev (standard deviation (σ) of the uncorrelated log-normal relaxed clock) (ESS = 19), rate.coefficientOfVariation (ESS = 56), YuleModel (ESS = 38) and birthrate (ESS = 59). In both analyses (ML and BI), Anacampserotaceae + Portulacaceae was resolved as sister to Cactaceae (Figure 1), and Pereskia s.s. and Leuenbergeria were resolved, although poorly (bs = 59) or moderately (pb = 0.99) supported, as a clade. The Cactaceae crown age was estimated at 28.23 +/− 3.71 Ma (Supplementary Figure S1 and Table S1), followed by a Leuenbergeria + Pereskia clade (15.19 Ma +/− 7.95 Ma). Cactoideae were strongly supported as sister to Opuntioideae (bs = 100, pb = 1.0), and Maihuenia was recovered as sister to that clade. Maihuenia diverged from the rest of Cactaceae at 27.22 +/− 3.87 Ma, while the remaining group Cactoideae + Opuntioideae had a crown age of 25.93 +/− 4.32 Ma. Cactoideae (including Blossfeldia + Cacteae and Core Cactoideae in our topology) diverged around 23.95 +/−4.07 Ma. Within Cactoideae, the diminutive Blossfeldia liliputana was recovered as sister to the rest of the clade. The North American, mostly desert-adapted Cacteae diverged around 17.52 Ma and were well supported as sister to the Calymmanthium + (Copiapoa + (Core Cactoideae I + Core Cactoideae II)) clades that consist of North, Central and South American species and that diverged around 20.82 Ma. Within Core Cactoideae I, Eulychnia and Corryocactus were subsequent sisters to the Pachycereinae + a well-supported clade (bs = 98) formed by Selenicereus, Armatocereus and Leptocereus, which diverged around 16.15 Ma. In Core Cactoideae II, Parodia was sister to the Trichocereeae + a poorly supported clade (bs = 58) formed by Rebutia, Eriocysce, Stetsonia, Arrojadoa, Pilosocereus and Melocactus. Core Cactoideae II diverged nearly in parallel with Core Cactoideae I, around 16.79 Ma.
The crown age for the well-supported Opuntioideae was recovered at 16.72 Ma (22.18–11.32 Ma), nearly paralleling the divergences of the tribe Cacteae and Core Cactoideae I and II. The young tribe Opuntieae, which diverged 7.92 +/− 3.94 Ma, was strongly supported as sister to a Tephrocacteae + Cylindropuntieae clade, which diverged from one another around 15.64 Ma (+/−5.48) Ma. The Caribbean endemic clade Consolea, which had a crown age of late Pleistocene origin (0.72 Ma), was resolved as sister to the rest of the Opuntieae, and the hyperdiverse genus Opuntia appears to have diverged around 4.38 Ma. Tacinga from the Brazilian caatinga biome (tropical dry forest) formed a sister clade to (Miqueliopuntia + Airampoa) + Opuntia. The Miqueliopuntia + Airampoa clade was very well supported (bs = 99), although its position as sister to Opuntia was poorly supported in our ML analysis (bs = 56) and well supported in our BI topology (pb = 1.0). Opuntia quitensis was resolved as sister to the rest of the species of Opuntia, and the southern South American clade, including O. quimilo and O. arechavaletae, was sister to the North American clade. The mostly hummingbird-pollinated Nopalea clade (sensu [55]) of SDTF was sister to the rest of the North American clades, most of which are desert-adapted. Maihueniopsis was sister to the rest of Tephrocacteae, and Pterocactus was sister to a Tephrocactus + (Austrocylindropuntia + Cumulopuntia) clade. As in Majure et al. [29], the leafy Quiabentia verticillata of the Chaco and Pereskiopsis of tropical dry forests of North America were subsequent sisters to a Micropuntia + (Cylindropuntia + Grusonia) clade. The crown ages for Maihueniopsis (8.63 Ma) and Tephrocactus (8.71 Ma) were older than the crown ages for Pterocactus (3.36 Ma) and the Austrocylindropuntia + Cumulopuntia clade (7.37 Ma) and older than those for subclades of Opuntieae and Cylindropuntieae. Grusonia diverged around 3.26 Ma, Cylindropuntia diverged 6.39 Ma, and Micropuntia, Pereskiopsis and Quiabentia diverged in the last 3.57–2.77 Ma (see Table 1).

3.2. Morphological Evolution

The ancestral growth form in Cactaceae under parsimony was reconstructed as herbs, shrubs or trees with equal probability, although all modern cacti are woody (see [62]). Both Cactoideae and Opuntioideae were reconstructed as ancestral shrubs but with numerous transitions to trees and several transitions to lianas or linaescent shrubs (Supplementary Figure S2A). Cylindrical stems were symplesiomorphic for Cactaceae, and flattened stems were synapomorphic for Opuntieae, although these reversed back to cylindrical stems in Miqueliopuntia (Figure 2A). Monopodial stems were plesiomorphic for Cactaceae, although transitions to sympodial stems occurred in some members of Cactoideae, and sympodial stems were predominant in Opuntioideae, although with a few transitions back to monopodial growth in that clade, such as in Consolea, Austrocylindropuntia, Perekiopsis, Quiabentia and Cylindropuntia leptocaulis (Figure 2B). Large (macroscopic) leaves were symplesiomorphic for Cactaceae, including Opuntioideae, and small (microscopic) leaves were a synapomorphy of Cactoideae (Figure 2C). Flattened leaves were symplesiomorphic in Cactaceae, and reduced, cylindrical leaves were synapomorphic for the Maihuenia (Cactoideae + Opuntioideae) clade. However, large, flattened leaves evolved separately in Quiabentia and Pereskiopsis (Figure 2D). Long-lived leaves were symplesiomorphic for Cactaceae, with ephemeral leaves being synapomorphic for Cactoideae + Opuntioideae. However, long-lived leaves were acquired three more times in Opuntioideae, in Austrocylindropuntia and Quiabentia and in Pereskiopsis (Figure 2E). Members of the tribe Opuntieae occurring in tropical dry forests, Chaco, Pampa or temperate forests (e.g., Elatae, Nopalea and Humifusa clades and O. pachyrrhiza) exhibited fewer areoles per stem face (<30) than those taxa occurring in drier, more open habitats, with the exception of the Antillean tree genus Consolea (with >30), which oftentimes has partially monopodial, flattened stems, as well as the small species of open, dry sandy soils of western Texas and northern Mexico, Opuntia arenaria with <30 (Supplementary Figure S2B), which has limited available space for areoles.

3.3. Ancestral Range Reconstruction

3.3.1. Range Defined Based on Habitat

Our RASP analysis showed that the best model was DEC+J (AICc_wt = 0.45), followed by DIVALIKE+J (AICc_wt = 0.42) (Supplementary Table S1). Based on these results, the habitat with higher speciation corresponded to deserts (106 events), followed by the tropical dry forest/SDTF (33). Most dispersal events happened from the desert to SDTF (10) and from the desert to temperate/subtropical forest (6). Overall, the desert habitat was the highest source of dispersal events (19), and the SDTF habitat was the main recipient of those dispersal events (13). Based on the DEC+J model results, the most recent common ancestor of Cactaceae evolved in a desert habitat (Figure 3A, node 348), with a small probability of an SDTF/desert origin. The Cactoideae + Opuntioideae clade (Figure 3A, node 246) and the Cactoideae (Figure 2A, node 237) evolved in the ancestral desert habitat range. Cactoideae showed dispersal events into SDTF (Figure 3A, nodes 215 and 227), temperate zones (Figure 3A, nodes 202 and 212) and the Chaco (Figure 3A, node 232), with a potential return to the desert (Figure 3A, node 219). The Cacteae clade originated in a desert habitat (Figure 3A, node 206), as did the Calymmanthium + Copiapoa + Core Cactoideae I + Core Cactoideae II clade (Figure 3A, node 235). Core Cactoideae I also originated in a desert habitat (Figure 3A, node 217), and Core Cactoideae II evolved in the Chaco (Figure 3A, node 232). From the Chaco, this clade dispersed into SDTF once (Figure 3A, node 227) and then back to the desert (Figure 3A, node 219).
According to the DEC+J model, Opuntioideae originated in a desert habitat (Figure 3B, nodes 345). We found support for the SDTF as the most probable origin of Opuntieae (Figure 3B, node 287), with subsequent dispersal events into Chaco (Figure 3B, node 247) and desert habitats (Figure 3B, node 281) and, finally, two dispersals into temperate/subtropical forest habitats (Figure 3B, node 271). According to our analysis, both Tephrocacteae and Cylindropuntieae clades evolved in a desert habitat (Figure 3C, node 344, 309 and 343). One dispersal of Tephrocacteae into SDTF occurred in Austrocylindropuntia (Figure 3, node 296). Cylindropuntieae included two early dispersal events: the first from a desert habitat to the Chaco region (Figure 3C, node 310) and the second one from the desert to SDTF (Figure 3C, node 313).

3.3.2. Range Defined Based on Ecoregions

Our Biogeobears analysis found the highest support for the BAYAREALIKE+J model (AICc_wt = 1), followed by the DIVALIKE+J model (AIC_wt = 8.20 × 10−7) (Supplementary Table S1). The corresponding Biogeographical Stochastic Mapping (BSM) analysis recovered the western North American deserts as the range with the most speciation events (68) followed by the Andean (41) and Caribbean regions (11). Most dispersal events happened from the Andes to three regions: the western North American deserts, the Caribbean and the Chaco, each with three events. Likewise, three dispersal events occurred from the Mexico–Central American SDTF to the western North American deserts. The BSM results also recovered the Andes as the source ecoregion of most dispersal events (14), followed by Mexico–Central American SDTF (7) and the Caribbean region (8). Additionally, the ecoregion that was the main recipient of dispersal events was the Caribbean region (8), followed by western North American deserts (7) and Mexico–Central American SDTF (7).
Based on the BAYAREALIKE+J results, the most recent common ancestor of Cactaceae had an Andean range (Supplementary Figure S3, node 191). The Leuenbergeria + Pereskia clade (Supplementary Figure S3, node 192) maintained the ancestral Andean range and subsequently dispersed to the Caribbean and Mexico–Central American SDTF (Supplementary Figure S3, node 193). This clade also included a dispersal to the Chaco region (Supplementary Figure S3, node 197) within Pereskia. The Cactoideae + Opuntioideae (Supplementary Figure S3, node 199) and the Cactoideae clade (Supplementary Figure S3, node 200) were reconstructed as originating in the ancestral Andean range. We then observed several range changes within the Cactoideae clade. The Cacteae clade originated in western North American deserts after the dispersal of a MRCA of that clade from the Andean region (Supplementary Figure S3, node 202), while its sister clade Core Cactaceae (Calymmanthium + Copiapoa + Cactoideae I + Core Cactoideae II) retained the Andean ancestral range (Supplementary Figure S3, nodes 217, 218 and 219). Core Cactoideae I also maintained the Andean ancestral range (Supplementary Figure S3, node 220), with several dispersals into the Caribbean region (Supplementary Figure S3, node 222) and western North American deserts (Supplementary Figure S3, node 227) and a potential dispersal back to the Andean range (Supplementary Figure S3). Core Cactoideae II appears to have evolved in the Chaco region (Supplementary Figure S3, node 231) with a dispersal to the Caribbean region (Supplementary Figure S3, node 241) and Eastern Highlands (Brazil—Caatinga) (Supplementary Figure S3, nodes 242 and 245), with potential movement back to the Andean region (Supplementary Figure S3).
The Opuntioideae clade (Supplementary Figure S3, node 246), as well as the Opuntieae (Supplementary Figure S3, node 247) and Tephrocacteae + Cylindropuntieae clades (Supplementary Figure S3, node 297), originated in the ancestral Andean range. We observed several dispersal events within Opuntieae: to the Caribbean region (Supplementary Figure S3, nodes 248 and 263), Eastern Highlands (Brazil—Caatinga) (Supplementary Figure S3, node 253), Chaco and Pampas (Supplementary Figure S3, node 261), western North American deserts (Supplementary Figure S3, node 260), Mexico–Central America SDTF (Supplementary Figure S3, node 265) and Eastern temperate forests (Supplementary Figure S3, node 287). The Tephrocacteae clade originated in the ancestral Andean range (Supplementary Figure S3, node 298), while Cylindropuntieae appears to have had a Chaco origin (Supplementary Figure S3 node 320), although this is weakly supported. Finally, the Pereskiopsis + the rest of Cylindropuntia subclade showed a range change to Mexico–Central America SDTF (Supplementary Figure S3, node 323) and then a shift into western North American deserts in the Micropuntia + Cylindropuntia and Grusonia clade.

4. Discussion

4.1. Phylogenetic Relationships in Cactaceae

The sister relationship of (Anacampserotaceae + Portulacaceae) + Cactaceae, as found here, has been recovered in several recent analyses with sufficient taxon sampling [18,20,21]. Although most analyses with sufficient taxon/data sampling have recovered Leuenbergeria and Pereskia as subsequent sisters to the rest of Cactaceae, our analyses recovered the two clades as sisters, although very poorly supported in ML analyses (bs = 59). It may be likely that the paucity of taxon sampling in our analyses could have affected our resulting topology, although Walker et al. [20] and Wang et al. [21] found high levels of incongruence among gene trees from transcriptome data around the Pereskia–Leuenbergeria node(s). So, the recalcitrance of this node does not appear to be ameliorated by using plastome data, at least when using just genes. Perhaps entire plastomes would provide better-supported topologies, along with the inclusion of more species from both clades. For example, the Central American Leuenbergeria lychnidiflora (not sampled here), which is sister to the rest of Leuenbergeria [26], may be key to obtaining a paraphyletic “Pereskia s.l.” Maihuenia has often been resolved as sister to Cactoideae [20,21,26,29]; however, our plastid gene dataset consistently resolved Maihuenia as sister to a Cactoideae + Opuntioideae clade. It is unclear whether the increased taxon sampling of Cactoideae in our analyses (Figure 1), as compared to previous analyses, may have resulted in this topology. Future work will need to more fully address the placement of Maihuenia.
Within Cactoideae, Blossfeldia was resolved as sister to the rest of the taxa sampled here, a placement in agreement with other phylogenetic studies [30]. As in Hernández-Hernández et al. [30], we recovered the tribe Cacteae as sister to the Core Cactoideae, which was well supported, and Calymmanthium and Copiapoa were subsequent sisters to the Core Cactoideae I + Core Cactoideae II clade. In Cacteae, as in Breslin et al. [48], we resolved three separate clades from the Mammilloid clade, Mammillaria, Coryphantha and Cochemiea s.l., but our sampling was not comprehensive enough to evaluate other more recent findings regarding generic delimitation [98]. Within Core Cactoideae I, Eulychnia was well supported as sister to the rest of the clade, a placement not previously supported. The structure of Core Cactoideae II was very similar to that described by Hernández-Hernández et al. [30], although with much poorer taxon sampling in our dataset.
Opuntioideae have most often been recovered in phylogenetic analyses as sister to Cactoideae [20,21,23,26,30,32,33], as we found here, although a recent plastome analysis by Yao et al. [15] recovered the Opuntioid clade as sister to the rest of Cactaceae, a seemingly anomalous placement. The Opuntioid clade comprises three major clades, the Opuntieae, Tephrocacteae and Cylindropuntieae. Most analyses to date have not resolved relationships among these three clades, or topologies have been poorly supported [30,32,54,59] or based on very poor taxon sampling [20,21]. Majure et al. [29], using plastome data, resolved Opuntieae as sister to a well-supported Tephrocacteae + Cylindropuntieae clade; however, both Opuntieae and Tephrocacteae were very poorly sampled. Our more comprehensive sampling here further lends support for Opuntieae as sister to a Tephrocacteae + Cylindropuntieae clade (bs = 90; Figure 1). Köhler et al. [35] likewise recovered this topology using several datasets derived from plastome data and a series of smaller datasets. Transcriptome datasets, however, have repeatedly recovered a Tephrocacteae + Opuntieae clade as sister to the Cylindropuntieae clade [20,21]. Likewise, a reduced dataset using the top five most highly informative plastid loci across Opuntioideae also recovered that topology [35]. What underlies these topological incongruences is currently unclear; however, it seems possible that selective pressures in loci derived from transcriptome data and homoplasy using rapidly evolving plastid genes that include intergenic spacers, such as in the five-locus dataset of Köhler et al. [35], could influence those differing topologies. The dataset implemented here is also not without its limitations, so to appropriately test this major incongruence among the three Opuntioid tribes, multiple, independent, single-copy nuclear loci should also be considered, such as in a hyb-seq approach [99].
In contrast to Majure et al. [55], Opuntia quitensis was resolved here as sister to the remaining species of Opuntia, including the South American (Elatae) clade, consisting of O. quimilo and O. arechavaletae. Majure et al. [55] recovered the South American clade as sister to the rest and O. quitensis as sister to the North American clade, although that placement was poorly supported. Likewise, the Nopalea clade within Opuntieae here was resolved as sister to the rest of the North American clades, whereas it was sister to the Basilares clade in previous analyses [55]. The Macrocentra clade here does not include O. santa-rita and its relatives, in contrast to previous analyses, and was recovered as sister to the Humifusa clade, although this was not well supported (bs = 64). Likewise, O. chlorotica was resolved outside of the O. santa-rita clade, in the Macrocentra clade, although that species is morphologically very similar to O. santa-rita. Opuntia guatemalensis, although morphologically slightly different from the other members of the hummingbird-pollinated members of the Nopalea clade, was still resolved inside of that clade as in Majure et al. [55], suggesting a transition back to insect pollination from bird pollination in that clade. Incongruencies between our current topology and those of Majure et al. [55] are likely a result of the increased resolution in our current dataset, as well as the use of combined plastid + nuclear DNA (ITS, ppc) in Majure et al. [55]. Species and clade relationships and competing topologies in Opuntieae are being tested further by Köhler et al. (in prep.).
Ritz et al. [59] resolved Maihueniopsis (bs = 69) as sister to Pterocactus, though this was poorly supported; however, our topology resolved Pterocactus as sister to an Austrocylindropuntia + Cumulopuntia (+ Tephrocactus) clade (bs = 76), which was moderately well supported. Although the Austrocylindropuntia + Cumulopuntia (+ Tephrocactus) clade was not well supported (bs = 66) in Ritz et al. [59], we also resolved that clade but with very high support (bs = 100). As in Ritz et al. [59], we resolved Maihueniopsis clavarioides and M. domeykoensis as subsequent sisters to the rest of the Maihueniopsis clade. We also resolved Tephrocactus bonnieae and T. molinensis in a clade, as well as T. aoracanthus, T. articulatus and T. alexanderi in a clade, as in Ritz et al. [59]. Species limits within Tephrocactus were recently tested by Las Peñas et al. [60], and species relationships in our analyses were nearly identical to their strict consensus tree, although their study included more taxa than what was used in our study. Our sampling of Pterocactus was extremely limited (to just two species), so we can say little about species relationships. However, Las Peñas and Bernardello [100] recently provided a detailed, species-level phylogeny and cytogenetic analysis of this mostly polyploid genus.
Our topology of Cylindropuntieae here was very similar to that described by Majure et al. [29], although we included fewer taxa in the current analysis, and clades were not as well supported as with nearly all plastome data. As in Majure et al. [29], we recovered the Great Basin endemic Micropuntia as sister to the Grusonia + Cylindropuntia clade, further confirming its placement outside of Grusonia.

4.2. Morphological Evolution and Ancestral Habitats

The flattened stems of Opuntieae are clearly synapomorphic for that clade (Figure 2A). In light of SDTF being the most likely putative ancestral area for that clade, flattened stems or large leaves would be necessary to compete with large-leaved species of trees and shrubs in those areas. Thus, the flattened cladodes could act to increase the surface area available for increased photosynthetic rates in those lower-light environments. Many species of Consolea have very thin stem segments, which, although long-lived, seem to be shed at a higher frequency than in other groups of desert-adapted species of Opuntia, for instance. Other members of the Opuntieae clade, including the tree members of the Nopalea clade and Brasiliopuntia (not sampled here) inhabiting SDTF, show some of the same characters. So, the large, flattened cladodes effectively act as broad leaves. The same can be seen in certain members of Cactoideae (not sampled here), such as Epiphyllyum and Schlumbergera, which inhabit low-light environments and produce flattened stem segments, presumably for the same purpose (although, developmentally, those flattened stems are quite different from those in Opuntieae).
Likewise, the number of areoles and/or spine production per cladode face appears to be correlated with habitat, with those species occurring in SDTF, Chaco and temperate/subtropical forest regions having far fewer areoles per cladode face (<30), as compared to desert species that produce higher numbers of areoles per cladode face (>30) and thus have the potential to produce more spines (Supplementary Figure S2B). This pattern has been observed in Cylindropuntieae and Tephrocacteae as well (Majure, upubl. data), but it has not yet been quantified. Certain members of the subfamily Cactoideae also appear to show this pattern, where more ribs (and thus potentially more areoles and spines) are produced in desert environments. The south-facing stem faces notably produce more and deeper ribs, which increases the stem area and can potentially affect photosynthetically active radiation (PAR) interception, stem temperature and CO2 uptake [101]. Nobel [102,103,104,105], in a series of experiments, showed that spines in cacti aided in regulating plant body temperature by reducing shortwave radiation on the stem and thus producing a boundary layer around the stem, which greatly impeded vastly fluctuating stem temperatures. Likewise, spines act to reflect incident PAR, thereby further decreasing potential stem heat loads. Therefore, the production of higher numbers of areoles and the potential for producing higher numbers of spines for protection against UV radiation and higher temperatures may be correlated with the desert environment, where more extreme temperatures are experienced. So, although Opuntieae may have evolved flattened stems to cope with low-light environments, they could compensate for the high amount of exposed stem surface by clothing their epidermis in spines. Another potential advantage to producing higher areole numbers could be an increase in the passive absorption of water via glochids [106], which are ubiquitous in the areoles of Opuntioideae.
Certain desert members of Opuntieae produce no spines at all (e.g., Opuntia basilaris, O. microdasys and O. rufida) and, on the contrary, produce a dense pubescence that clothes the epidermis and presumably aids in absorbing shortwave radiation, which again helps to regulate plant body temperature [107]. The exhibition of purple betalain pigments by the stems, as always occurs in some prickly pears, such as Opuntia santa-rita and O. macrocentra, has been suggested by Gibson and Nobel [107] to act to reflect incident PAR, thereby further protecting the plant body from damaging temperatures. However, the effects of pigmentation on cacti are poorly studied.
As proposed by Majure et al. [29], and supported here with much broader taxon sampling, the large, persistent, flattened leaf blades of Quiabentia and Pereskiopsis have been acquired separately from cylindrical, ephemeral-leaved ancestors (Figure 2D,E). Likewise, Austrocylindropuntia has acquired persistent leaves separately, and those leaves, although appearing totally cylindrical, show some modifications similar to a bifacial leaf [108]. These large, persistent leaves appear to be correlated with the adaptation to life in SDTF and/or Chaco habitats from desert-adapted ancestors with greatly reduced and ephemeral leaves. From a gross morphological point of view, these taxa have essentially reacquired Pereskia/Leuenbergeria-like leaves for adaptation to more or less the same types of broad-leaf, tropical dry forests, where those leaves aid to increase photosynthetic capacity.
Bailey [109] analyzed the anatomy of Pereskiopsis and Quiabentia leaves and determined that they were anatomically distinct from the leaves of other leafy Cactaceae, such as “Pereskia s.l.”. Pereskiopsis and Quiabentia have palmate or pseudopalmate venation, as opposed to pinnate venation, as is exhibited by Pereskia and Leuenbergeria. Likewise, the leaves of Pereskiopsis and Quiabentia are truly succulent, meaning that they produce associated parenchymatous tissue, increasing the thickness of the leaves for significant water storage. Bailey [110] analyzed the leaves of Austrocylindropuntia subulata and found a similar, although more condensed, palmate venation to that of Pereskiopsis and Quiabentia. He also mentioned the semi-bifacial structure of the leaves, as is seen in cross-section, with the vascular bundles mostly restricted to the adaxial surface instead of the entire leaf becoming adaxialized, as in the truly cylindrical leaves of other Opuntioideae, such as Opuntia s.s.
Hernández-Hernández et al. [24] concluded that the growth forms of all other cacti and the subfamily Cactoideae were not comparable and thus excluded Maihuenia, Opuntioideae and Pereskia s.l. from previous analyses of morphological evolution, contrasting that of the growth forms of Cactoideae. However, there is no great distinction between these groups, as most Cactoideae are either trees or shrubs, regardless of branching patterns, etc. Likewise, taxa such as Armatocereus, Cephalocereus (in part; [111]), Leptocereus and Rhipsalis (Cactoideae) have nearly identical growth forms to those of most Opuntioideae, showing determinate, sympodial growth of the stem segments, as seen in our reconstructions here (Figure 2B, Supplementary Figure S2A). Likewise, certain Opuntioideae possess indeterminate, monopodial growth (e.g., Austrocylindropuntia, Brasiliopuntia, Consolea, Cylindropuntia leptocaulis (at least initially), Pereskiopsis and Tacinga funalis; Figure 2B). So, the great distinction of growth forms among these groups is mostly artificial, as all cacti share a basic body plan having alternate spiral leaf phyllotaxy (these are sometimes coalesced into ribs, as in many Cactoideae and Grusonia bradtiana in Opuntioideae; see also [62]). Therefore, we emphasize that variations on a common theme, such as the growth forms associated with succulence across most Cactaceae [112], likely impacted the morphological evolution of Cactaceae as a whole, not just Cactoideae.

4.3. Biogeography of Opuntioideae

The ancestral areas for the Cactaceae as a whole, as well as Opuntioideae, Tephrocacteae and Cylindropuntieae, were at least in part reconstructed as being the desert, based, of course, on the modern distribution of the species sampled here and an admittedly broad generalization of desert habitats across the Americas. However, according to what we know regarding the formation of deserts in the Americas, as well as the putative ages of these clades (15–28 my), we must infer that the MRCAs of these groups evolved in edaphically arid habitats that perhaps were not as extensive as modern desert regions [113]. Desert formation to the extent that we see them today would account for the rapid radiation of these groups in the mid-Miocene and into Plio- and Pleistocene epochs [23,114].
Our ancestral area reconstruction based on ecoregions revealed, as in other analyses (e.g., [24]), that the Andes were the likely center of origin of Cactaceae. From Andean South America, the clade dispersed essentially throughout the rest of the Americas (Figure 4). This is also true for Opuntioideae, with a putative origin in the Andes and then movement into other dry areas of the Americas. Tephrocacteae, however, remained in the Andes and significantly diversified there, in contrast to Cylindropuntieae and Opuntieae, which diversified much more substantially outside of the Andes [29,55]. There have been numerous dispersals into western North America, such as in Opuntieae, Cylindropuntieae [29,55], Cacteae [43] and Core Cactaceae II [115], and likewise into the Antilles [50,58,115] from South America (Figure 4). So, there has been a repeated pattern of movement out of South America during the diversification of Cactaceae, in general. This has likely been fostered by the expansive drylands of western North America [113] and the seasonally dry tropical forests of the Antilles and Mesoamerica [116].

5. Conclusions

Opuntioideae evolved in the Miocene in the desert regions of South America and, from there, moved into SDTF and temperate regions, including spreading north into western North American deserts (Figure 4), where the bulk of the diversity was generated. Within Opuntioideae, Tephrocacteae and Cylindropuntieae form a well-supported sister clade to Opuntieae. Opuntioideae exhibit ancestral features in cacti, including large (macroscopic) leaves; however, the production of large, long-lived, photosynthetically active leaves in Austrocylindropuntia, Pereskiopsis and Quiabentia represents homoplasy, having been acquired secondarily, likely as an adaptation to SDTF and Chaco vegetation. The flattened stem segments of the tribe Opuntieae are a synapomorphy for that group and are likely an adaptation for competition in dense SDTF, the putative ancestral habitat for the clade. Areole production appears to increase in hotter, drier conditions within the tribe Opuntieae, which would enable these plants to produce higher numbers of spines to protect stems from UV radiation and associated overheating. Species relationships and major clade relationships are mostly resolved with plastome datasets, which show promise for resolving recalcitrant nodes across the family.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/d15040570/s1. Figure S1: BEAST analysis showing crown ages for major clades and posterior probability support; Figure S2: Morphological evolution of (A) growth form and (B) areole number in Opuntieae; Figure S3: Ancestral geographic area based on ecoregions using BAYAREALIKE+J model in BioGeobears; Table S1: BioGeoBears model test results for both habitat and ecoregion analyses; Section S1: Accessions used in our plastome analysis.

Author Contributions

Conceptualization, L.C.M.; methodology, L.C.M. and S.A.; formal analysis, L.C.M. and S.A.; investigation, L.C.M.; resources, M.A.B., R.P.-M. and S.F.; data curation, L.C.M. and S.A.; writing—original draft preparation, L.C.M. and S.A.; writing—review and editing, L.C.M., S.A., M.A.B., M.K., R.P.-M. and S.F.; visualization, L.C.M. and S.A.; supervision, L.C.M.; project administration, L.C.M.; funding acquisition, L.C.M. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded in part by the National Science Foundation, DEB 1735604.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Our plastid gene dataset, taxon coding and trees generated are available on FigShare (10.6084/m9.figshare.22211935).

Acknowledgments

This work was made possible in part through the Desert Botanical Garden Living collection and financial support from the Desert Botanical Garden. Financial support was also provided in part by the National Science Foundation (DEB 1735604). Permits for material collected for this project were provided by El Ministereo del Medio Ambiente y Recursos Naturales, Dominican Republic, the US National Park Service (Lake Mead National Recreation Area and Big Bend National Park), Arizona, California and Nevada Bureau of Land Management, as well as Big Pine Key Deer Refuge, Florida. The Desert Botanical Garden Herbarium (DES), Arizona State University Herbarium (ASU) and the University of Florida Herbarium (FLAS) serve as repositories for many of the specimens used in our analyses. Lastly, we would like to thank two anonymous reviewers for providing comments on a previous version of this paper.

Conflicts of Interest

The authors have no conflict of interest for the data generated and presented in this study. The funders had no role in the design of the study; in the collection, analyses or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

References

  1. Britton, N.L.; Rose, J.N. The Cactaceae. Descriptions and Illustrations of Plants of the Cactus Family; Carnegie Institution of Washington D.C.: New York, NY, USA, 1919; Volume 1. [Google Scholar]
  2. Benson, L. The Cacti of the United States and Canada; Stanford University Press: Stanford, CA, USA, 1982. [Google Scholar]
  3. Anderson, E. The Cactus Family; Timber Press: Portland, OR, USA, 2001. [Google Scholar]
  4. Croizat, L. Manual of Phytogeography; Junk: Hague, The Netherlands, 1952. [Google Scholar]
  5. Buxbaum, F.; Kakteenleben. Eine Biologische Plauderei fur Jeden Naturfreund; A Philler Verlag: Minden, Germany, 1980. [Google Scholar]
  6. Barthlott, W. Biogeography and evolution in neo-and paleotropical Rhipsalinae. In Dispersal and Distribution; Kubitski, K., Ed.; Verlag Paul Parey: Hamburg, Germany, 1983; pp. 241–248. [Google Scholar]
  7. Backeberg, C. Cactaceae; Jahrbücher der DKG., Teil 2, Juni 1942: 55, Cactaceae Lindley; Systematische Übersicht (Neubearbeitung) mit Beschreibungsschlüssel. 1942. Available online: https://www.cactuspro.com/biblio_fichiers/pdf/CactJahr/CactJahr1941.pdf (accessed on 1 November 2022).
  8. Renner, S. Plant dispersal across the tropical Atlantic by wind and sea current. Int. J. Plant Sci. 2004, 165, S23–S33. [Google Scholar] [CrossRef]
  9. Cota-Sánchez, J.H.; Bomfim-Patrício, M.C. Seed morphology, polyploidy and the evolutionary history of the epiphytic cactus Rhipsalis baccifera (Cactaceae). Polibotánica 2010, 29, 107–129. [Google Scholar]
  10. Guerrero, P.; Majure, L.C.; Bustamante, E.; Hernández-Hernández, T. Phylogenetic relationships and evolutionary trends in the cactus family. J. Hered. 2018, 110, 4–21. [Google Scholar] [CrossRef] [PubMed]
  11. Ocampo, G.; Columbus, J.T. Molecular phylogenetics of suborder Cactineae (Caryophyllales), including insights into photosynthetic diversification and historical biogeography. Am. J. Bot. 2010, 97, 1827–1847. [Google Scholar] [CrossRef] [PubMed]
  12. Soltis, D.E.; Smith, S.A.; Cellinese, N.; Wurdack, K.J.; Tank, D.C.; Brockington, S.F.; Refulio-Rodriguez, N.F.; Walker, J.B.; Moore, M.J.; Carlsward, B.S.; et al. Angiosperm phylogeny: 17 genes, 640 taxa. Am. J. Bot 2011, 98, 704–730. [Google Scholar] [CrossRef]
  13. Brockington, S.F.; Yang, Y.; Gandia-Herrero, F.; Covshoff, S.; Hibberd, J.M.; Sage, R.F.; Wong, G.K.S.; Moore, M.J.; Smith, S.A. Lineage-specific gene radiations underlie the evolution of novel betalain pigmentation in Caryophyllales. New Phytol. 2015, 207, 1170–1180. [Google Scholar] [CrossRef]
  14. Yang, Y.; Moore, M.J.; Brockington, S.F.; Soltis, D.E.; Wong, G.K.S.; Carpenter, E.J.; Zhang, Y.; Chen, L.; Yan, Z.; Xie, Y.; et al. Dissecting molecular evolution in the highly diverse plant clade Caryophyllales using transcriptome sequencing. Mol. Phylogent. Evol. 2015, 32, 2001–2014. [Google Scholar] [CrossRef]
  15. Yao, G.; Jin, J.J.; Li, H.T.; Yang, J.B.; Mandala, V.S.; Croley, M.; Mostow, R.; Douglas, N.A.; Chase, M.W.; Christenhusz, J.M.; et al. Plastid phylogenomic insights into the evolution of Caryophyllales. Mol. Phylogent. Evol. 2019, 134, 74–86. [Google Scholar] [CrossRef]
  16. Goolsby, E.W.; Moore, A.J.; Hancock, L.P.; De Vos, J.M.; Edwards, E.J. Molecular evolution of key metabolic genes during transition to C4 and CAM photosynthesis. Am. J. Bot. 2018, 105, 602–613. [Google Scholar] [CrossRef]
  17. Nyffeler, R. The closest relatives of cacti: Insights from phylogenetic analyses of chloroplast and mitochondrial sequences with special emphasis on relationships in the tribe Anacampseroteae. Am. J. Bot. 2007, 94, 89–101. [Google Scholar] [CrossRef]
  18. Moore, A.J.; de Vos, J.M.; Hancock, L.P.; Goolsby, E.; Edwards, E.J. Targeted enrichment of large gene families for phylogenetic inference: Phylogeny and molecular evolution of photosynthesis genes in the Portullugo clade (Caryophyllales). Syst. Biol. 2017, 67, 367–383. [Google Scholar] [CrossRef] [PubMed]
  19. Yang, Y.; Moore, M.J.; Brockington, S.F.; Mikenas, J.; Olivieri, J.; Walker, J.F.; Smith, S.A. Improved transcriptome sampling pinpoints 26 paleopolyploidy events in Caryophyllales, including two paleo-allopolyploidy events. New Phytol. 2018, 217, 855–870. [Google Scholar] [CrossRef]
  20. Walker, J.F.; Yang, Y.; Feng, T.; Timoneda, A.; Mikenas, J.; Hutchison, V.; Edwards, C.; Wang, N.; Ahluwalia, S.; Olivieri, J.; et al. From cacti to carnivores: Improved phylotranscriptomic sampling and hierarchical homology inference provides further insight to the evolution of Caryophyllales. Am. J. Bot. 2018, 105, 1–17. [Google Scholar] [CrossRef]
  21. Wang, N.; Yang, Y.; Moore, M.J.; Brockington, S.F.; Walker, J.F.; Brown, J.W.; Liang, B.; Feng, T.; Edwards, C.; Mikenas, J.; et al. Evolution of Portulacineae marked by adaptation to harsh environments, gene tree conflict, and gene family expansion. Mol. Biol. Evol. 2018, 36, 112–126. [Google Scholar] [CrossRef]
  22. Hershkovitz, M.A.; Zimmer, E.A. On the evolutionary origins of the cacti. Taxon 1997, 46, 217–232. [Google Scholar] [CrossRef]
  23. Arakaki, M.; Christin, P.-A.; Nyffeler, R.; Lendel, A.; Eggli, U.; Ogburn, R.M.; Spriggs, E.; Moore, M.J.; Edwards, E.J. Contemporaneous and recent radiations of the world’s major succulent plant lineages. Proc. Natl. Acad. Sci. USA 2011, 108, 8379–8384. [Google Scholar] [CrossRef] [PubMed]
  24. Hernández-Hernández, T.; Brown, J.W.; Schlumpberger, B.O.; Eguiarte, L.E.; Magallón, S. Beyond aridification: Multiple explanations for the elevated diversification of cacti in the New World succulent biome. New Phytol. 2014, 202, 1382–1397. [Google Scholar] [CrossRef]
  25. Rodrigues Silva, G.S.; Antonelli, A.; Lendel, A.; de Moraes, E.M. The impact of Quaternary climate change on the diversification and population dynamics of a South American cactus species. J. Biogeogr. 2018, 45, 76–88. [Google Scholar] [CrossRef]
  26. Edwards, E.J.; Nyffeler, R.; Donoghue, M.J. Basal cactus phylogeny: Implications of Pereskia (Cactaceae) paraphyly for the transition to the cactus life form. Am. J. Bot. 2005, 92, 1177–1188. [Google Scholar] [CrossRef] [PubMed]
  27. Butterworth, C.; Edwards, E.J. Investigating Pereskia and the earliest divergences in Cactaceae. Haseltonia 2008, 14, 46–53. [Google Scholar] [CrossRef]
  28. Nyffeler, R.; Eggli, U.A. farewell to dated ideas and concepts: Molecular phylogenetics and a revised suprageneric classification of the family Cactaceae. Schummania 2010, 6, 109–149. [Google Scholar]
  29. Majure, L.C.; Baker, M.A.; Cloud-Hughes, M.; Salywon, A.; Neubig, K.M. Phylogenomics in Cactaceae: A case study using the chollas sensu lato (Cylindropuntieae, Opuntioideae) reveals a common pattern out of the Chihuahuan and Sonoran deserts. Am. J. Bot. 2019, 106, 1327–1345. [Google Scholar] [CrossRef]
  30. Hernández-Hernández, T.; Hernández, H.M.; De-Nova, J.A.; Puente, R.; Eguiarte, L.E.; Magallón, S. Phylogenetic relationships and evolution of growth form in Cactaceae (Caryophyllales, Eudicotyledoneae). Amer. J. Bot. 2011, 98, 44–61. [Google Scholar] [CrossRef]
  31. Wallace, R.S. Molecular systematic study of the Cactaceae: Using chloroplast DNA variation to elucidate cactus phylogeny. Bradleya 1995, 13, 1–12. [Google Scholar] [CrossRef]
  32. Wallace, R.S.; Dickie, S.L. Systematic implications of chloroplast DNA sequences variation in the Opuntioideae. In Studies in the Opuntioideae (Cactaceae); Hunt, D.R., Taylor, N.P., Eds.; David Hunt: Milborne Port, Sherborne, UK, 2002. [Google Scholar]
  33. Crozier, B. Systematics of Cactaceae Juss: Phylogeny, cpDNA Evolution, and Classification with Emphasis on the Genus Mammillaria Haw. Ph.D. Thesis, University of Texas, Austin, TX, USA, 2005. [Google Scholar]
  34. Bárcenas, R.T.; Yesson, C.; Hawkins, J. Molecular systematics of the Cactaceae. Cladistics 2011, 27, 470–489. [Google Scholar] [CrossRef]
  35. Köhler, M.; Reginato, M.; Souza-Chies, T.T.; Majure, L.C. Next-generation sequencing across Opuntioideae (Cactaceae): Insights into plastome structural variation and phylogenetic markers in a prickly group. Front. Pl. Sci. 2020, 11, 729. [Google Scholar] [CrossRef] [PubMed]
  36. Arias, S.; Terrazas, T.; Cameron, K. Phylogenetic analysis of Pachycereus (Cactaceae, Pachycereeae) based on chloroplast and nuclear sequences. Syst. Bot. 2003, 28, 547–557. [Google Scholar]
  37. Arias, S.; Terrazas, T.; Arreola-Nava, H.J.; Vazquez-Sanchez, M.; Cameron, K.M. Phylogenetic relationships in Peniocereus (Cactaceae) inferred from plastid DNA sequence data. J. Plant Res. 2005, 118, 317–328. [Google Scholar] [CrossRef]
  38. Butterworth, C.A.; Wallace, R.S. Phylogenetic studies of Mammillaria (Cactaceae)—Insights from chloroplast sequence variation and hypothesis testing using the parametric bootstrap. Am. J. Bot. 2004, 91, 1086–1098. [Google Scholar] [CrossRef]
  39. Calvente, A.; Zappi, D.C.; Forest, F.; Lohmann, L.G. Molecular phylogeny, evolution, and biogeography of South American epiphytic cacti. Int. J. Plant Sci. 2011, 172, 902–914. [Google Scholar] [CrossRef]
  40. Calvente, A.; Moraes, E.M.; Lavor, P.; Bonatelli, I.A.; Nacaguma, P.; Versieux, L.M.; Taylor, N.P.; Zappi, D.C. Phylogenetic analyses of Pilosocereus (Cactaceae) inferred from plastid and nuclear sequences. Bot. J. Lin. Soc. 2017, 183, 25–38. [Google Scholar] [CrossRef]
  41. Demaio, P.H.; Barfuss, M.H.; Kiesling, R.; Till, W.; Chiapella, J.O. Molecular phylogeny of Gymnocalycium (Cactaceae): Assessment of alternative infrageneric systems, a new subgenus, and trends in the evolution of the genus. Am. J. Bot. 2011, 98, 1841–1854. [Google Scholar] [CrossRef]
  42. Franck, A.R.; Cochrane, B.J.; Garey, J.R. Phylogeny, biogeography, and infrageneric classification of Harrisia (Cactaceae). Syst. Bot. 2013, 38, 210–223. [Google Scholar] [CrossRef]
  43. Vázquez-Sánchez, M.; Terrazas, T.; Arias, S.; Ochoterena, H. Molecular phylogeny, origin and taxonomic implications of the tribe Cacteae (Cactaceae). Syst. Biod. 2013, 11, 103–116. [Google Scholar] [CrossRef]
  44. Sánchez, D.; Arias, S.; Terrazas, T. Phylogenetic relationships in Echinocereus (Cactaceae, Cactoideae). Syst. Bot. 2014, 39, 1183–1196. [Google Scholar] [CrossRef]
  45. Vázquez-Lobo, A.; Morales, G.A.; Arias, S.; Golubov, J.; Hernández-Hernández, T.; Mandujano, M.C. Phylogeny and biogeographic history of Astrophytum (Cactaceae). Syst. Bot. 2016, 40, 1022–1030. [Google Scholar] [CrossRef]
  46. Vargas-Luna, M.D.; Hernández-Ledesma, P.; Majure, L.C.; Puente, R.; Hernández, H.M.; Bárcenas, R.T. Splitting Echinocactus: Morphological and molecular evidence support the recognition of Homalocephala as a distinct genus in the Cacteae. PhytoKeys 2018, 111, 31–59. [Google Scholar] [CrossRef]
  47. Barrios, D.; Arias, S.; González-Torres, L.R.; Majure, L.C. Phylogeny and taxonomy of the Antillean endemic genus Leptocereus (Cactaceae) inferred from chloroplast markers and morphological evidence. Pl. Syst. Evol. 2020, 306, 63. [Google Scholar] [CrossRef]
  48. Breslin, P.; Wojciechowski, M.; Majure, L.C. Molecular phylogeny of the Mammilloid clade (Cactaceae) of Baja California and adjacent regions: Resolving the monophyly of Mammillaria with new combinations in Cochemiea. Taxon 2021, 70, 308–323. [Google Scholar] [CrossRef]
  49. Majure, L.C.; Clase, T.; Encarnación, Y.; Peguero, B.; Ho, K.; Barrios, D. Phylogenetics of Leptocereus (Cactaceae) on Hispaniola: Clarifying species limits in the L. weingartianus complex and a new species from the Sierra de Bahoruco. Phytokeys 2021, 172, 17–37. [Google Scholar] [CrossRef]
  50. Majure, L.C.; Barrios, D.; Díaz, E.; Bacci, L.F.; Encarnación, Y. Phylogenomics of the Caribbean Melocacti: Cryptic species and multiple invasions. Taxon 2022, 71, 993–1012. [Google Scholar] [CrossRef]
  51. Hunt, D.R. That’s Opuntia, that was! Succul. Plant Res. 2002, 6, 245–248. [Google Scholar]
  52. Hunt, D.R. An interim checklist of the subfamily Opuntioideae (Cactaceae) in the Caribbean region and South America. Succul. Plant Res. 2014, 8, 201–223. [Google Scholar]
  53. Griffith, M.P. Grusonia pulchella reclassification and its impact on the genus Grusonia: Morphological and molecular evidence. Haseltonia 2002, 9, 86–93. [Google Scholar]
  54. Griffith, M.P.; Porter, J.M. Phylogeny of Opuntioideae. Int. J. Plant Sci. 2009, 170, 107–116. [Google Scholar] [CrossRef]
  55. Majure, L.C.; Puente, R.; Griffith, M.P.; Judd, W.S.; Soltis, P.S.; Soltis, D.E. Phylogeny of Opuntia s.s. (Cactaceae): Clade delineation, geographic origins, and reticulate evolution. Am. J. Bot. 2012, 99, 847–864. [Google Scholar] [CrossRef]
  56. Majure, L.C.; Soltis, D.E.; Soltis, P.S.; Judd, W.S. A case of mistaken identity, Opuntia abjecta, long-lost in synonymy under the Caribbean species, O. triacantha, and a reassessment of the enigmatic O. cubensis. Brittonia 2014, 66, 118–130. [Google Scholar] [CrossRef]
  57. Majure, L.C.; Puente, R. Phylogenetic relationships and morphological evolution in Opuntia s. str. and closely related members of tribe Opuntieae. Succul. Plant Res. 2014, 8, 9–30. [Google Scholar]
  58. Majure, L.C.D.; Barrios, E.; Díaz, B.; Zumwalde, W.T.; Negrón-Ortiz, V. Pleistocene drying underlies the evolutionary history of the Caribbean endemic, insular giant, Consolea (Opuntioideae). Am. J. Bot. 2021, 108, 200–215. [Google Scholar] [CrossRef]
  59. Ritz, C.M.; Reiker, J.; Charles, G.; Hoxey, P.; Hunt, D.; Lowry, M.; Stuppy, W.; Taylor, N. Molecular phylogeny and character evolution in terete-stemmed Andean opuntias (Cactaceae–Opuntioideae). Molec. Phylogen. Evol. 2012, 65, 668–681. [Google Scholar] [CrossRef]
  60. Las Peñas, M.L.; Kiesling, R.; Bernardello, G. Phylogenetic reconstruction of the genus Tephrocactus (Cactaceae) based on molecular, morphological and cytogenetical data. Taxon 2019, 68, 714–730. [Google Scholar] [CrossRef]
  61. Bárcenas, R.T. A molecular phylogenetic approach to the systematics of Cylindropuntieae (Opuntioideae, Cactaceae). Cladistics 2016, 32, 351–359. [Google Scholar] [CrossRef] [PubMed]
  62. Mauseth, J.D. Structure-function relationships in highly modified shoots of Cactaceae. Ann. Bot. 2006, 98, 901–926. [Google Scholar] [CrossRef] [PubMed]
  63. Mauseth, J.D. Tiny but complex foliage leaves occur in many “leafless” cacti (Cactaceae). Int. J. Plant Sci. 2007, 168, 845–853. [Google Scholar] [CrossRef]
  64. Nobel, P.S.; Bobich, E.G. Environmental biology. In Cacti: Biology and Uses; Nobel, P.S., Ed.; University of California Press: Berkeley, CA, USA, 2002; pp. 57–74. [Google Scholar]
  65. Winter, K.; Garcia, M.; Holtum, J.A.M. Drought-stress-induced up-regulation of CAM in seedlings of a tropical cactus, Opuntia elatior, operating predominantly in the C3 mode. J. Exp. Bot. 2011, 62, 4037–4042. [Google Scholar] [CrossRef] [PubMed]
  66. Mauseth, J.D. An introduction to cactus areoles part II. Cactus Succ. J. 2017, 89, 219–229. [Google Scholar] [CrossRef]
  67. Majure, L.C.; Puente, R.; Pinkava, D.J. Miscellaneous chromosome counts in Opuntieae DC. (Cactaceae) with a compilation of counts for the group. Haseltonia 2012, 18, 67–78. [Google Scholar] [CrossRef]
  68. Baker, M.A.; Pinkava, D.J. Chromosome numbers in some cacti of Western North America—IX. Haseltonia 2018, 25, 4–28. [Google Scholar] [CrossRef]
  69. Liu, X.; Yang, H.; Zhao, J.; Zhou, B.; Li, T.; Xiang, B. The complete chloroplast genome sequence of the folk medicinal and vegetable plant purslane (Portulaca oleracea L.). J. Hort. Sci. Biotech. 2018, 93, 356–365. [Google Scholar] [CrossRef]
  70. Neubig, K.M.; Whitten, W.M.; Abbott, J.R.; Elliott, S.; Soltis, D.E.; Soltis, P.S. Variables affecting DNA preservation in archival plant specimens. In DNA Banking for the 21st Century: Proceedings of the US Workshop on DNA Banking; Applequist, W.L., Campbell., L.M., Eds.; Missouri Botanical Garden; William L. Brown Center: St. Louis, MI, USA, 2014; pp. 81–112. [Google Scholar]
  71. Katoh, K.; Standley, D.M. A simple method to control over-alignment in the MAFFT multiple sequence alignment program. Bioinformatics 2016, 32, 1933–1942. [Google Scholar] [CrossRef]
  72. Stamatakis, A. RaxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014, 30, 1312–1313. [Google Scholar] [CrossRef] [PubMed]
  73. Bouckaert, R.; Vaughan, T.G.; Barido-Sottani, J.; Duchêne, S.; Fourment, M.; Gavryushkina, A.; Heled, J.; Jones, G.; Kuhnert, D.; De Maio, N.; et al. BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 2019, 15, e1006650. [Google Scholar] [CrossRef] [PubMed]
  74. Lanfear, R.; Frandsen, P.B.; Wright, A.M.; Senfeld, T.; Calcott, B. PartitionFinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol. 2017, 34, 772–773. [Google Scholar] [CrossRef] [PubMed]
  75. Darriba, D.; Taboada, G.L.; Doallo, R.; Posada, D. jModelTest 2: More models, new heuristics and parallel computing. Nat. Methods 2012, 9, 772. [Google Scholar] [CrossRef] [PubMed]
  76. Miller, M.A.; Pfeifferand, W.; Schwartz, T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop; GCE: New Orleans, LA, USA, 2010; pp. 1–8. [Google Scholar]
  77. Smith, S.A.; O’Meara, B.C. treePL: Divergence time estimation using penalized likelihood for large phylogenies. Bioinformatics 2012, 28, 2689–2690. [Google Scholar] [CrossRef]
  78. Rambaut, A.; Drummond, A. FigTree: Tree Figure Drawing Tool, v1. 4.2; Institute of Evolutionary Biology, University of Edinburgh: Edinburgh, UK, 2012.
  79. Rambaut, A.; Drummond, A.J. LogCombiner, v2. 6.2.; Institute of Evolutionary Biology, University of Edinburgh: Edinburgh, UK, 2014.
  80. Rambaut, A.; Drummond, A.J. TreeAnnotator, v2.6.2. MCMC Output Analysis. 2020. Available online: https://www.beast2.org/treeannotator/ (accessed on 1 March 2021).
  81. Mauseth, J.D. Some cacti produce large, ephemeral foliage leaves when they flower. Int. J. Pl. Sci. 2022, 183, 119–127. [Google Scholar] [CrossRef]
  82. Maddison, W.P.; Maddison, D.R. Mesquite: A Modular System for Evolutionary Analysis, Version 2.75. 2017. Available online: http://mesquiteproject.org (accessed on 1 March 2021).
  83. Yu, Y.; Harris, A.J.; Blair, C.; He, X. RASP (Reconstruct Ancestral State in Phylogenies): A tool for historical biogeography. Mol. Phylogenetics Evol. 2015, 87, 46–49. [Google Scholar] [CrossRef]
  84. Matzke, N.J. BioGeoBEARS: BioGeography with Bayesian (and Likelihood) Evolutionary Analysis in R Scripts; University of California: Berkeley, CA, USA, 2013. [Google Scholar]
  85. Matzke, N.J. Probabilistic historical biogeography: New models for founder-event speciation, imperfect detection, and fossils allow improved accuracy and model-testing. Frontiers Biogeogr. 2013, 54, 242–248. [Google Scholar]
  86. Matzke, N.J. Model Selection in Historical Biogeography Reveals that Founder-event Speciation is a Crucial Process in Island Clades. Syst. Biol. 2014, 63, 951–970. [Google Scholar] [CrossRef]
  87. R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing: Vienna, Austria. 2020. Available online: https://www.R-project.org/ (accessed on 1 March 2021).
  88. Dupin, J.; Matzke, N.J.; Särkinen, T.; Knapp, S.; Olmstead, R.G.; Bohs, L.; Smith, S.D. Bayesian estimation of the global biogeographical history of the Solanaceae. J. Biogeogr. 2017, 44, 887–899. [Google Scholar] [CrossRef]
  89. Matzke, N.J. Stochastic Mapping under Biogeographical Models. PhyloWiki BioGeoBEARS website. 2016. Available online: https://phylo.wikidot.com/biogeobears#stochastic_mapping (accessed on 1 March 2021).
  90. Griffith, G.E.; Omernik, J.M.; Azevedo, S.H. Ecological Classification of the Western Hemisphere; Unpublished Report; Environmental Protection Agency, Western Ecology Division: Corvallis, OR, USA, 1998; 49p.
  91. Ree, R.H.; Smith, S.A. Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Syst. Biol. 2008, 57, 4–14. [Google Scholar] [CrossRef]
  92. Massana, K.A.; Beaulieu, J.M.; Matzke, N.J.; O’Meara, B.C. Non-null effects of the null range in biogeographic models: Exploring parameter estimation in the dec model. BioRxiv 2015. [Google Scholar] [CrossRef]
  93. Ronquist, F. Duspersal-vicariance analysis: A new approach to the quantification of historical biogeography. Syst. Biol. 1997, 46, 195–203. [Google Scholar] [CrossRef]
  94. Landis, M.J.; Matzke, N.J.; Moore, B.R.; Huelsenbeck, J.P. Bayesian analysis of biogeography when the number of areas is large. Syst. Biol. 2013, 62, 789–804. [Google Scholar] [CrossRef] [PubMed]
  95. Burnham, K.P.; Anderson, D.R. Multimodel inference: Understanding AIC and BIC in model selection. Soc. Method Res. 2004, 33, 261–304. [Google Scholar] [CrossRef]
  96. Ree, R.H.; Sanmartín, I. Conceptual and statistical problems with the DEC+J model of founder-event speciation and its comparison with DEC via model selection. J. Biogeogr. 2018, 45, 741–749. [Google Scholar] [CrossRef]
  97. Matzke, N.J. Statistical comparison of DEC and DEC+J is identical to comparison of two ClaSSE submodels and is therefore valid. J. Biogeogr. 2022, 49, 1805–1824. [Google Scholar] [CrossRef]
  98. Sánchez, D.; Vázquez-Benítez, B.; Vázquez-Sánchez, M.; Aquino, D.; Arias, S. Phylogenetic relationsjhips in Coryphantha and implications on Pelecyphora and Escobaria (Cacteae, Cactoideae, Cactaceae). Phytokeys 2022, 188, 115–165. [Google Scholar] [CrossRef]
  99. Acha, S.; Majure, L.C. A new approach using targeted sequence capture for phylogenomic studies across Cactaceae. Genes 2022, 13, 350. [Google Scholar] [CrossRef]
  100. Las Peñas, M.L.; Bernardello, G. Divergence time estimation and mapping of morphological and cytogenetical data in the southern South American geophyte genus Pterocactus (Cactaceae). Taxon 2021, 70, 477–698. [Google Scholar] [CrossRef]
  101. Lewis, D.A.; Nobel, P.S. Thermal energy exchange model and water loss of a barrel cactus, Ferocactus acanthodes. Plant Physiol. 1977, 60, 609–616. [Google Scholar] [CrossRef] [PubMed]
  102. Nobel, P.S. Surface temperatures of cacti—Influences of environmental and morphological factors. Ecology 1978, 59, 986–996. [Google Scholar] [CrossRef]
  103. Nobel, P.S. Interception of photosynthetically active radiation by cacti of different morphologies. Oecologia 1980, 45, 160–166. [Google Scholar] [CrossRef] [PubMed]
  104. Nobel, P.S. Morphology, surface temperatures, and northern limits of columnar cacti of the Sonoran Desert. Ecology 1980, 61, 1–7. [Google Scholar] [CrossRef]
  105. Nobel, P.S. Spine influences on PAR interception, stem temperature and nocturnal acid acumulation by cacti. Plant Cell Environ. 1983, 6, 153–159. [Google Scholar] [CrossRef]
  106. Ju, J.; Bai, H.; Zheng, Y.; Zhao, T.; Fang, R.; Jiang, L. A mult-structural and multi-functional integrated fog collection system in cactus. Nat. Commun. 2012, 3, 1247. [Google Scholar] [CrossRef]
  107. Gibson, A.C.; Nobel, P.S. The Cactus Primer; Harvard University Press: Cambridge, MA, USA, 1986. [Google Scholar]
  108. Boke, N.H. Histogenesis of the leaf and areole in Opuntia cylindrica. Am. J. Bot. 1944, 31, 299–316. [Google Scholar] [CrossRef]
  109. Bailey, I.W. Comparative anatomy of the leaf-bearing Cactaceae, I. Foliar vasculature of Pereskia, Pereskiopsis and Quiabentia. J. Arnold Arbor. 1960, 41, 341–356. [Google Scholar] [CrossRef]
  110. Bailey, I.W. Comparative anatomy of the leaf-bearing Cactaceae, XVII. Preliminary observations on the problem of transitions from broad to terete leaves. J. Arnold Arbor. 1968, 49, 370–376. [Google Scholar] [CrossRef]
  111. Tapia, H.J.; Bárcenas-Arguello, M.L.; Terrazas, T. Phylogeny and circumscription of Cephalocereus (Cactaceae) based on molecular and morphological evidence. Syst. Bot. 2017, 42, 1–15. [Google Scholar] [CrossRef]
  112. Nyffeler, R.; Eggli, U.; Ogburn, M.; Edwards, E. Variations on a theme: Repeated evolution of succulent life forms in the Portulacineae (Caryophyllales). Haseltonia 2008, 14, 26–36. [Google Scholar] [CrossRef]
  113. Wilson, J.S.; Pitts, J.P. Illuminating the lack of consensus among descriptions of earth history data in the North American deserts: A resource for biologists. Prog. Phys. Geogr. 2010, 34, 419–441. [Google Scholar] [CrossRef]
  114. Breslin, P.; Wojciechowski, M.; Majure, L.C. Remarkably rapid, recent diversification of Cochemiea and Mammillaria (Cactaceae) in the Baja California, Mexico Region. Am. J. Bot. 2022, 109, 1472–1487. [Google Scholar] [CrossRef] [PubMed]
  115. Lavor, P.; Calvente, A.; Versieux, L.M.; Sanmartin, I. Bayesian spatio-temporal reconstruction reveals rapid diversification and Pleistocene range expansion in the widespread columnar cactus Pilosocereus. J. Biogeogr. 2018, 46, 238–250. [Google Scholar] [CrossRef]
  116. Pennington, R.T.; Prado, D.E.; Pendry, C.A. Neotropical seasonally dry forests and Quaternary vegetation changes. J. Biogeogr. 2000, 27, 261–273. [Google Scholar] [CrossRef]
Diversity 15 00570 g001 550
Figure 1. Maximum likelihood topology from RAxML. Cactaceae were recovered as sister to an Anacampserotaceae + Portulacaceae clade. Pereskia and Leuenbergeria were poorly supported as a clade, and Maihuenia was supported as sister to a Cactoideae + Opuntioideae clade. Opuntioideae was well supported and consisted of an Opuntieae + (Cylindropuntieae + Tephrocacteae) clade. Bootstrap support (bs) is given above branches. * = 100 bs, and support <100 is given. Photos taken by L.C. Majure.
Figure 1. Maximum likelihood topology from RAxML. Cactaceae were recovered as sister to an Anacampserotaceae + Portulacaceae clade. Pereskia and Leuenbergeria were poorly supported as a clade, and Maihuenia was supported as sister to a Cactoideae + Opuntioideae clade. Opuntioideae was well supported and consisted of an Opuntieae + (Cylindropuntieae + Tephrocacteae) clade. Bootstrap support (bs) is given above branches. * = 100 bs, and support <100 is given. Photos taken by L.C. Majure.
Diversity 15 00570 g001
Diversity 15 00570 g002 550
Figure 2. Morphological evolution in Cactaceae. (A) Cylindrical stems (black) were plesiomorphic, and Opuntieae displayed the synapomorphy (white) of flattened stems. (B) Monopodial stems (white) were plesiomorphic, and sympodial stems (black) evolved several times in Cactoideae, as well as in Opuntioideae, where there were also several changes back to monopodial growth. (C) Large, macroscopic (vegetative) leaves were plesiomorphic (black) in Cactaceae, but near-total leaf reduction was synapomorphic for Cactoideae. (D) Flattened (bifacial) leaves were ancestral in Cactaceae (black) and then re-evolved in Cylindropuntieae, and (E) long-lived leaves (black) were ancestral and then re-evolved in both Tephrocacteae and Cylindropuntieae.
Figure 2. Morphological evolution in Cactaceae. (A) Cylindrical stems (black) were plesiomorphic, and Opuntieae displayed the synapomorphy (white) of flattened stems. (B) Monopodial stems (white) were plesiomorphic, and sympodial stems (black) evolved several times in Cactoideae, as well as in Opuntioideae, where there were also several changes back to monopodial growth. (C) Large, macroscopic (vegetative) leaves were plesiomorphic (black) in Cactaceae, but near-total leaf reduction was synapomorphic for Cactoideae. (D) Flattened (bifacial) leaves were ancestral in Cactaceae (black) and then re-evolved in Cylindropuntieae, and (E) long-lived leaves (black) were ancestral and then re-evolved in both Tephrocacteae and Cylindropuntieae.
Diversity 15 00570 g002
Diversity 15 00570 g003a 550Diversity 15 00570 g003b 550Diversity 15 00570 g003c 550
Figure 3. Ancestral habitat reconstruction using our BEAST chronogram. (A) Cactaceae were reconstructed as evolving in a desert environment, while the Pereskia clade originated in SDTF, Core Cactoideae I moved into SDTF from the desert, and Core Cactoideae II were reconstructed as evolving in the Chaco before moving into SDTF and back into the desert. (B) Opuntieae were reconstructed as evolving in SDTF and, from there, moving into the desert, Chaco and temperate forest, while Tephrocacteae were reconstructed as evolving in the desert and then moving into SDTF, and (C) Cylindropuntieae evolved in a desert habitat and then moved into the Chaco and SDTF.
Figure 3. Ancestral habitat reconstruction using our BEAST chronogram. (A) Cactaceae were reconstructed as evolving in a desert environment, while the Pereskia clade originated in SDTF, Core Cactoideae I moved into SDTF from the desert, and Core Cactoideae II were reconstructed as evolving in the Chaco before moving into SDTF and back into the desert. (B) Opuntieae were reconstructed as evolving in SDTF and, from there, moving into the desert, Chaco and temperate forest, while Tephrocacteae were reconstructed as evolving in the desert and then moving into SDTF, and (C) Cylindropuntieae evolved in a desert habitat and then moved into the Chaco and SDTF.
Diversity 15 00570 g003aDiversity 15 00570 g003bDiversity 15 00570 g003c
Diversity 15 00570 g004 550
Figure 4. Map of putative dispersal events of Cactaceae across the Americas. Arrows indicate the directionality of dispersal. Cactaceae originated in arid areas of South America, and there were movements between the desert and SDTF on several occasions. Numerous dispersals occurred out of South America into the Caribbean region from the desert, Chaco and SDTF and into western North America, mostly from desert habitats. Movement from the desert to the Chaco and then into SDTF occurred within South America, and movement from SDTF to desert and desert to temp./suptrop. forest occurred in North America.
Figure 4. Map of putative dispersal events of Cactaceae across the Americas. Arrows indicate the directionality of dispersal. Cactaceae originated in arid areas of South America, and there were movements between the desert and SDTF on several occasions. Numerous dispersals occurred out of South America into the Caribbean region from the desert, Chaco and SDTF and into western North America, mostly from desert habitats. Movement from the desert to the Chaco and then into SDTF occurred within South America, and movement from SDTF to desert and desert to temp./suptrop. forest occurred in North America.
Diversity 15 00570 g004
Table
Table 1. Crown ages and confidence intervals from our BEAST analysis.
Table 1. Crown ages and confidence intervals from our BEAST analysis.
CladeCrown AgeCI
Pereskia + Leuenbergeria15.197.24–27.83
Maihuenia + the rest27.2223.35–31.23
Cactoideae25.9319.88–28.16
Cacteae17.5312.32–23.25
Core Cactoideae I17.5312.32–23.25
Core Cactoideae II20.8316.39–25.72
Opuntioideae16.7311.32–22.18
Opuntieae7.923.98–12.11
Tacinga1.750.16–4.51
Miqueliopuntia + Tunilla3.531.51–5.88
Consolea0.730.14–1.64
Opuntia4.392.52–6.43
Tephrocacteae13.348.74–18-86
Tephrocactus8.724.65–13.08
Pterocactus3.370.45–6.95
Austrocylindropuntia + Cumulopuntia7.373.73–11.54
Maihueniopsis8.653.83–13.78
Cylindropuntieae12.27.86–16.55
Quiabentia3.580.37–7.66
Pereskiopsis30.87–5.82
Micropuntia2.770.38–5.54
Cylindropuntia6.43.86–9.05
Grusonia3.261.41–5.77
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Majure, L.C.; Achá, S.; Baker, M.A.; Puente-Martínez, R.; Köhler, M.; Fehlberg, S. Phylogenomics of One of the World’s Most Intriguing Groups of CAM Plants, the Opuntioids (Opuntioideae: Cactaceae): Adaptation to Tropical Dry Forests Helped Drive Prominent Morphological Features in the Clade. Diversity 2023, 15, 570. https://doi.org/10.3390/d15040570

AMA Style

Majure LC, Achá S, Baker MA, Puente-Martínez R, Köhler M, Fehlberg S. Phylogenomics of One of the World’s Most Intriguing Groups of CAM Plants, the Opuntioids (Opuntioideae: Cactaceae): Adaptation to Tropical Dry Forests Helped Drive Prominent Morphological Features in the Clade. Diversity. 2023; 15(4):570. https://doi.org/10.3390/d15040570

Chicago/Turabian Style

Majure, Lucas C., Serena Achá, Marc A. Baker, Raul Puente-Martínez, Matias Köhler, and Shannon Fehlberg. 2023. "Phylogenomics of One of the World’s Most Intriguing Groups of CAM Plants, the Opuntioids (Opuntioideae: Cactaceae): Adaptation to Tropical Dry Forests Helped Drive Prominent Morphological Features in the Clade" Diversity 15, no. 4: 570. https://doi.org/10.3390/d15040570

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop