Aloe vera supports a substantial global trade yet its wild origins, and explanations for its popularity over 500 related Aloe species in one of the world’s largest succulent groups, have remained uncertain. We developed an explicit phylogenetic framework to explore links between the rich traditions of medicinal use and leaf succulence in aloes.
The phylogenetic hypothesis clarifies the origins of Aloe vera to the Arabian Peninsula at the northernmost limits of the range for aloes. The genus Aloe originated in southern Africa ~16 million years ago and underwent two major radiations driven by different speciation processes, giving rise to the extraordinary diversity known today. Large, succulent leaves typical of medicinal aloes arose during the most recent diversification ~10 million years ago and are strongly correlated to the phylogeny and to the likelihood of a species being used for medicine. A significant, albeit weak, phylogenetic signal is evident in the medicinal uses of aloes, suggesting that the properties for which they are valued do not occur randomly across the branches of the phylogenetic tree.
Phylogenetic investigation of plant use and leaf succulence among aloes has yielded new explanations for the extraordinary market dominance of Aloe vera. The industry preference for Aloe vera appears to be due to its proximity to important historic trade routes, and early introduction to trade and cultivation. Well-developed succulent leaf mesophyll tissue, an adaptive feature that likely contributed to the ecological success of the genus Aloe, is the main predictor for medicinal use among Aloe species, whereas evolutionary loss of succulence tends to be associated with losses of medicinal use. Phylogenetic analyses of plant use offer potential to understand patterns in the value of global plant diversity.
The succulent leaf tissue of Aloe vera is a globally important commodity, with an estimated annual market of $13 billion [1]. The ‘gel’ tissue—polysaccharide-rich inner leaf mesophyll—provides a reservoir of water to sustain photosynthesis during droughts, and has been ascribed multiple bioactive properties associated with its use for skincare and digestive health [2]. Aloe vera has supported a thriving trade for thousands of years [3] and is arguably one of the most popular plants known in cultivation today, yet its origins in the wild have long been speculated. We have established that at least 25% of aloes (~120 species) are used for medicine yet fewer than 10 Aloe species are traded commercially, and these are used primarily for the purgative leaf exudate and on much lesser scales than Aloe vera (e.g. Aloe ferox in South Africa and Aloe arborescens in Asia) [4]. The immense market dominance of Aloe vera over other species of Aloe is not fully explained by available phytochemical evidence [5,6]. The extent to which the value of Aloe vera may be a consequence of evolutionary processes of selection and speciation, resulting in apparently unique properties and phylogenetic isolation, has not previously been considered.
Aloe (>500 species) is by far the most speciose of the six genera known collectively as aloes, which include Aloiampelos (7 species), Aloidendron (6 species), Aristaloe (1 species), Gonialoe (3 species) and Kumara (2 species). They are iconic in the African flora, and occur predominantly in eastern sub-Saharan Africa, and on the Arabian Peninsula, Madagascar and western Indian Ocean islands. Succulent plants are usually associated with arid environments; although numerous aloes occur in the drylands of Africa, they are also abundantly represented in tropical and subtropical vegetation infrequently impacted by drought. All aloes possess some degree of leaf succulence, as well as crassulacean acid metabolism (CAM) and a thick, waxy cuticle common in plants exhibiting a succulent syndrome [7]. Most are habitat specialists with narrow ranges and extraordinary rates of endemism, from an estimated 70% in southern Africa, 90% in Ethiopia, to 100% on Madagascar [8]. These centres of diversity coincide alarmingly with Africa’s biodiversity Hotspots, where a highly endemic biota is under substantial threat of extinction [9]. Risks posed by extensive habitat destruction and other threats to their survival are reflected by the inclusion of all aloes, except Aloe vera, in the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). The species-level diversity, ecological importance and threats to aloes place them among the world’s most important succulent plant lineages, other examples of which are ice plants (Aizoaceae), cacti (Cactaceae) and Agave (Agavaceae) [10]. Phylogenetic studies of related groups have focussed on the South African endemic Haworthia (e.g. [11,12]), whereas aloes have received little attention (but see [13]), and the origins and diversification of Aloe have remained unclear. It has therefore not been possible to determine whether Aloe vera is phylogenetically distinct from its many relatives, nor whether such phylogenetic distance may account for any potentially unique properties underpinning the value of the succulent leaf tissue.
Phylogenetic prediction is emerging as a promising tool for exploring correlations between the phylogenetic diversity and useful attributes of medicinal plants [14-17]. Rich biocultural traditions surround the use of aloe leaves for medicine, cosmetics, digestive health and general wellbeing [4]. Two natural products are derived from the leaves: carbohydrate-rich succulent leaf mesophyll tissue, applied topically to the skin or taken internally for digestion; and exudate, a liquid matrix high in phenolic compounds and most often used as a potent purgative, or in veterinary medicine (see [18]). The literature describing these uses is an untapped resource for understanding plant use in an evolutionary context, and in particular the extraordinary case of Aloe vera, which is used almost exclusively for its succulent leaf tissue. One point of interest is whether leaf succulence in aloes, which ranges from barely succulent in some species to very fleshy in others, could influence their use.
We aimed to explore the Aloe vera ‘phenomenon’ [5] by combining the largest ever phylogenetic hypothesis for the aloes with predictive methods. We used this to infer a scenario for their evolution, addressing a persistent gap in the understanding of global succulent plant diversity and biogeography. Links between the medicinal usefulness of aloes, their phylogenetic history, and extent of leaf succulence were evaluated by identifying evolutionary correlations and phylogenetic signal in uses and habit. Our comprehensive sampling represents the full morphological and geographical diversity of the aloes, and enabled the origins, geographical range evolution and divergence times of Aloe and relatives to be inferred. We synthesized our findings to determine whether the global value of Aloe vera can be better explained by evolutionary distinctiveness or by historical anthropogenic factors.
A dataset was assembled representing seven plastid and nuclear DNA regions in 239 taxa in Xanthorrhoeaceae, including 197 species in the genera Aloe, Aloidendron, Aloiampelos, Aristaloe, Gonialoe and Kumara. We generated 480 new sequences from leaf or floral specimens collected from natural populations or from curated living collections and DNA banks held primarily at the Royal Botanic Gardens, Kew. A further 279 sequences were obtained from GenBank (ncbi.nlm.nih.gov/genbank/), including 93 rbcL and 64 psbA sequences. Agapanthus africanus (Amaryllidaceae) was used as the outgroup taxon in all analyses.
Total genomic DNA was isolated from fresh plant material (ca. 1 g) or specimens dried in silica gel (ca. 0.3 g) using a modified CTAB protocol [19] or the Qiagen DNeasy kit (Qiagen, Copenhagen). Sequences of ITS, matK and trnL-F were amplified using methodology previously described by [6]. The trnQ-rps16 region was amplified with the primers trnQ(UUG)Aloe (5′-ATCTTRATACAATGTGATCCAC-3′; this study) and rps16x1 [20]. Sequences from the complementary strands were obtained for all taxa whenever possible, using the BigDye Terminator v3.1 on a 3730 DNA Analyzer (Applied Biosystems/Hitachi). Sequences were assembled in Sequencher 4.8 (Gene Codes, Ann Arbor) and submitted to GenBank (Additional file 1). Sequences were aligned automatically using MUSCLE [21] implemented with default settings in SeaView v4.2.12 [22], and adjusted manually in BioEdit v7.1.11 [23]. The DNA regions were aligned separately before the data were concatenated using an R [24] script to produce a final dataset comprising 240 taxa and 6732 nucleotides in seven DNA regions.
We used Bayesian inference, maximum likelihood and parsimony to produce a phylogenetic hypothesis for Aloe and allied genera, using single-partition (ITS, matK, rps16, psbA, rbcL, trnL-F intron and spacer) and combined datasets. We ran all analyses on the Cyber Infrastructure for Phylogenetic Research (CIPRES) portal [25]. Separate parsimony analyses of the ITS (175 taxa, 799 nucleotides) and plastid (231 taxa, 5933 nucleotides) datasets were undertaken with the parsimony ratchet implemented in PAUPRat [26], to check for strongly supported phylogenetic conflicts (bootstrap percentages >75), before proceeding with analyses based on a total evidence approach using all characters. A maximum likelihood analysis, comprising 1000 bootstrap replicates followed by a heuristic tree search, was executed in RAxML [27] with each partition assigned specific parameters under the recommended GTRCAT model. An additional 530 gaps and indels in the combined dataset of all DNA regions were coded using the algorithm described by [28] in the FastGap v1.2 interface [29]. Finally, we ran a Bayesian analysis of the combined dataset with gaps coded in MrBayes v3.1.2 [30]. Best-fitting models for each data partition for Bayesian inference were identified using the Akaike Information Criterion calculated in Modeltest v3.8 [31]. The Hasegawa, Kishino and Yano (HKY) model with gamma-shaped distribution of rate heterogeneity among sites (HKY + G) was selected for the ITS, matK, trnQ-rps16 and trnL-F data partitions, while the General Time Reversible (GTR) model with gamma distribution of rate heterogeneity among sites was selected for psbA (GTR + G), and with a proportion of invariable sites (GTR + I + G) for rbcL. For the Bayesian analysis, the parameters were unlinked between loci and four Metropolis Coupled Markov Chains with heating increments of 0.2 were run for 50 million generations and sampled every 1000th generation. The resulting parameters were summarised in Tracer 1.5.0 [32]. A quarter of the least likely trees were discarded, and a majority rule consensus tree with branch supports expressed as posterior probabilities (PP) was produced from the remaining trees.
The aloe plant has been revered for centuries for its healing properties and versatile uses But where did this succulent originate? Tracing the roots of the aloe provides a fascinating look into the intertwining histories of ancient civilizations across Africa, Europe and Asia
Early History and Ancient Uses
The aloe plant has been utilized for over 5000 years One of the first recorded uses comes from ancient Egypt, where aloe was dubbed the “plant of immortality” The Egyptians used the aloe’s gel to treat wounds, infections and skin conditions. Aloe was also used in the embalming process for pharaohs.
Ancient Greek and Roman physicians like Dioscorides wrote of aloe’s ability to heal burns, wounds and other discomforts. In India’s Ayurvedic medicine, aloe was known as “ghritkumari” and used to treat constipation, skin diseases and female infertility.
Trading Along the Silk Road
As early as the 4th century BC aloe was trafficked along trade routes like the Red Sea and Silk Road. Traders likely carried aloe from Socotra an island off the coast of Somalia known as “the island of aloes.”
Merchants bought and sold aloe in bustling marketplaces from Persia to China. This extensive trade helped aloe plants spread across Europe and Asia.
Arrival in Europe
In the 15th century, European explorers like Christopher Columbus seized on aloe’s popularity. They carried aloe westward from Africa, Asia and the Middle East to Europe.
Spanish explorers introduced aloe to the Caribbean and Americas in the 16th century. They relied on the plant’s healing powers to treat the wounds and burns of weary travelers.
Botanical Classification
Early botanists first classified aloe as a lily due to their similar appearance. In the 18th century, French botanist Charles Linnaeus identified over 200 aloe species and created the plant’s official botanical name “Aloe vera.”
Further genetic testing has since regrouped different aloe species under the family name Asphodelaceae. There are now over 500 identified aloe species.
Modern Cultivation
Today, aloe is cultivated globally as an ornamental plant and for agricultural uses. The succulent thrives in warm, dry climates with sandy soil. Major producers include China, Mexico, South Africa, and the United States.
Aloe’s clear gel is extracted from the leaves to manufacture medicines, cosmetics, and health drinks. The plant also holds cultural and religious significance in some African and Indian ceremonies.
From ancient Egypt to modern day, aloe has spread across continents over thousands of years thanks to its versatile healing powers. The resilient succulent continues to be an important cultural, medicinal and agricultural plant whose origins span diverse cultures across Africa, Europe and Asia. Tracing aloe’s history provides insight into the interconnectedness of ancient civilizations.
Phylogenetic signal in utility and habit
We interrogated a dataset of over 1400 use records from the literature [18] to investigate phylogenetic signal in the uses of aloes. Data were coded according to the Economic Botany Data Standard [43] from which two categories of use were considered. In the first category, we combined all TDWG Level 1 data to yield a discrete binary character describing any documented use, while the second comprised data in the TDWG Level 2 Medicines category. General use (e.g. for food, materials, social purposes, etc.) and medicinal use specifically were scored as present (=1) or absent (=0) in each of the terminal taxa. Records describing a plant as not used are unusual in the ethnobotanical literature, and hence in all cases 0 indicated a lack of reported use, rather than definitive knowledge of no use. The consensus (allcompat) tree inferred by Bayesian analysis with gaps coded was pruned to 197 species representing Aloe, Aloiampelos, Aloidendron, Aristaloe, Gonialoe and Kumara.
We calculated phylogenetic signal using the D metric [44], a measure specifically developed for quantifying phylogenetic signal in binary characters, implemented in the R package caper [45]. D compares the number of observed changes in a trait over a phylogeny with the number that would be expected under two alternative simulated scenarios: one where there is strong phylogenetic dependence and the trait has evolved via a gradual Brownian motion model of evolution, and the second where there is no phylogenetic dependence and the trait is randomly scattered across the species, regardless of phylogeny. The D metric generates a value that usually lies between 0 and 1, where a value of 1 indicates that the trait has evolved in essentially a random manner (i.e. no phylogenetic signal), and 0 indicates that the trait is highly correlated with phylogeny, in a manner predicted by Brownian motion. Tests for significant differences from D = 1 (no phylogenetic signal) are derived by simulating the random distribution of the trait among species 1000 times to generate a null distribution for the D statistic. We conducted the analysis in two ways, one using just the consensus phylogeny, and the second using 1000 trees selected at random from the Bayesian posterior distribution calculating median values for D and associated P values.
The putative contribution of leaf succulence to the ‘usefulness’ of aloes was explored using a phylogenetic comparative approach. A character set describing the extent of water-storing mesophyll tissue in the leaves was assembled from species descriptions [46-48] and observations of leaf morphology in aloes. Species were broadly scored as ‘succulent’ or ‘barely succulent’ and additionally classified as barely succulent shrubs (the grass aloes, Aloe section Leptaloe), succulent shrubs (Aristaloe, Gonialoe and most of Aloe), branching trees (Aloidendron, Kumara) and scrambling shrubs with variably succulent leaves (Aloiampelos). These were visualised on the Bayesian consensus tree by reconstructing the ancestral states of three characters (succulence, habit and medicinal use), scored as binary traits, under the parsimony optimisation in Mesquite [49].
For calculation of phylogenetic signal using the D metric in these traits, they were coded as four separate dummy binary variables (e.g. succulence: 0 = no, 1 = yes). Pairwise comparison tests [50] were used to assess possible evolutionary correlations between habit and documented uses generally and medicinal uses specifically (dependent variables). This method takes phylogenetically independent pairs of species and observes any correlated differences in the states of two binary characters. For every gain or loss in one character (in this case, the measure of leaf succulence), it assesses whether there is an associated loss, gain or no change in the other (medicinal or general use), and compares any patterns with those expected if the second character were randomly distributed on the phylogeny. Pairwise comparison calculations were carried out using Mesquite [49]. As with our D metric calculations, to account for uncertainty in the phylogenetic topology and weak branch supports, we ran all the analyses on the Bayesian consensus (allcompat) topology (using 100 randomly selected sets of pairwise comparisons) and on a random sample of 1000 trees from the Bayesian posterior distribution, calculating median probability values associated with the correlation.
Our phylogenetic analyses of >7 kb plastid and nuclear characters (6732 nucleotides and 550 gaps) in ca. 40% of Aloe species substantiate current understanding of taxonomic relationships in Xanthorrhoeaceae subfamily Asphodeloideae [11,12,51] and divergence times within Asparagales [33] (Figure 1, Additional files 2 and 3). We sampled 26 genera and 240 species in Xanthorrhoeaceae, using a total evidence approach despite sequence data for some taxa being incomplete (Additional files 1 and 4). The effects of missing data on phylogenetic analyses have been widely debated, but there is convincing evidence for the accurate phylogenetic placement of taxa with considerable missing data (summarised by [52]). Model-based methods of phylogenetic inference perform better than parsimony in estimating trees from datasets with missing data [53,54], and we therefore based subsequent analyses on the Bayesian phylogenetic inference (Additional file 3). Low levels of genetic polymorphisms, taxonomic complexities, and the number of inaccessible, narrowly distributed species challenge the study of aloes; this is the first phylogeny to include >10% of Aloe species. Parsimony and maximum likelihood topologies (trees not shown) compared well to the Bayesian tree used in downstream analyses. Branching tree aloes (Aloidendron) are basal to the remainder of the alooids. A clade comprising the Cape endemic genus Kumara and Haworthia s.s. is sister to Aloiampelos, which is in turn sister to Aloe. Within the large Aloe clade (184 species), well-supported terminal branches highlight species-level relationships but the clades, which will ultimately underpin a taxonomic revision, are incompletely resolved. The placement of Aloiampelos juddii at the base of the alooid topology, on a branch sister to Kumara-Haworthia, warrants further investigation of reciprocal monophyly in Aloiampelos. We included four members of Astroloba, two Tulista, three Haworthiopsis and four Haworthia in our study and recovered these as paraphyletic with varying support. The haworthioid taxa were, until recently [12], phylogenetically problematic (e.g. [11]).
Subfamilies and genera of Xanthorrhoeaceae. Summary phylogram with Bayesian posterior probabilities (>0.5) above branches; red branches represent the six genera known collectively as aloes: Aloe, Aristaloe, Gonialoe, Kumara, Aloiampelos and Aloidendron.
Biogeographic scenario for Aloe. Distribution and biogeographic scenario for Aloe inferred from nucleotide and plastid data for 228 taxa in Xanthorrhoeaceae subfamily Asphodeloideae. Enlarged map shows the natural distribution of Aloe, with northernmost limits indicated by dashed line. Direction and timing of diversification events inferred from ancestral state reconstruction and penalised likelihood dating are shown by arrows. Histograms show branch-based (dispersal and extinction) and node-based (vicariance and peripheral isolations) events in speciation processes since the divergence of the Aloe crown group ~16 Ma.
Bayesian consensus tree for Aloe. Core Aloe clade from a Bayesian analysis of Xanthorrhoeaceae highlighting relationships of interest in the biogeographical scenario. Inset shows representative variation in the extent of leaf succulence among aloes: a, Aloiampelos ciliaris; b, Aloidendron eminens; c, Kumara plicatilis; d, Aloe vera; e, Aloe marlothii.
Bayesian consensus tree for Aloe (continued from Figure 3 ).
Divergence time estimates and biogeographic scenario
Divergence times were estimated using a penalised likelihood (PL) approach previously applied in Hyacinthaceae, a related family in Asparagales, as described by [33]. In the absence of fossil data for aloes and related genera, analyses were constrained to the mean age of 34.2 Ma inferred for the crown node of Asphodeloideae in a recent study of all Asparagales families [34]. Due to the computational demands of analyses on the full Xanthorrhoeaceae dataset and our focus on the aloes (Aloe, Aloiampelos, Aloidendron, Aristaloe, Gonialoe and Kumara), we excluded subfamilies Xanthorrhoeoideae and Hemerocallidoideae from subsequent analyses and pruned the Bayesian consensus tree to 228 species in Asphodeloideae. The penalised likelihood method [35] was run on 1000 randomly selected trees from the Bayesian stationary distribution and summarised on the consensus tree [33]. The optimal rate smoothing value for this dataset was determined by cross validation on the pruned Bayesian consensus tree, using the Truncated Newton algorithm (S = 5) implemented in r8s v 1.8 [36]. The outgroup taxon was pruned prior to the estimation of divergence times, as required by r8s. Mean age values and 95% confidence intervals for the nodes on the Bayesian consensus tree were computed in TreeAnnotator [37].
A biogeographic scenario for the aloes was inferred using the dispersal-extinction-cladogenesis (DEC) likelihood model implemented in Lagrange v2.0.1 [38]. Species distribution data were compiled from authoritative checklists for Asphodeloideae [39,40] and standardised according to the Taxonomic Data Working Group (TDWG) guidelines [41]. We defined eight areas based on the statistically-delimited biogeographical regions of Africa, incorporating the faunal and floral diversity of the continent, described recently by [42]. For subfamily Asphodeloideae, Arabia, Madagascar and Eurasia were added to the Southern African, Zambezian and Congolian regions, together with expanded Ethiopian-Somalian and Saharan-Sudanian regions. Assigning species to areas was straightforward due to the typically narrow distribution of most Aloe species, and because neighbouring areas are separated by physical barriers or marked differences in climatic conditions. Ancestral area reconstructions in Lagrange [38] were performed on the dated consensus (allcompat) tree obtained from the penalised likelihood analysis. In brief, ancestral areas were computed at each node of the tree under the DEC likelihood model, following a method described in detail by [33]. Ancestral areas with a relative probability >1 were combined with the node age and lengths of the descendent branches on the tree to infer the frequency and nature of transition events between ancestral and descendant nodes [33]. The resulting biogeographic scenario was visualised on the dated Bayesian consensus tree using pie charts showing the likelihoods of all possible ancestral areas per node for subfamily Asphodeloideae.
Why? Tell Me Why! Aloe: The Miracle Plant
FAQ
What is the origin of the aloe vera plant?
Who was the first person to discover aloe vera?
Is there scientific evidence for aloe vera?
What is the historical use of aloe vera?
When was aloe vera first discovered?
Historically, we may never know when Aloe Vera’s wellness applications were first discovered as they likely predate written history. We do know of the 6000 years old carvings of the plant discovered in Egypt and, at some point after, became a common burial offering or gift to deceased pharaohs and its remnants are found tombs.
Where does the aloe vera plant come from?
In this article, we will explore the origin of the Aloe Vera Plant. The aloe vera plant belongs to the Asphodelaceae family and is native to Africa. Specifically, it’s believed that it originated in Sudan or South Africa.
Why did ancient Egyptians use aloe vera?
Ancient Egyptians were one of the first civilizations recorded using aloe vera plants extensively. They called it “the plant of immortality” due to its ability to heal wounds quickly and effectively without leaving any scars behind.
What did Columbus discover about aloe vera?
He wrote about his discoveries and about the medicinal uses of Aloe vera, ranging from treating burns to combating acne to soothing gastrointestinal conditions. Much of the research that he did is still believed today. Aloe vera was included in the cargo sent along with Columbus when he discovered the New World.