Pereskia and the origin of the cactus life-form

The cactus life-form is cited as an example of a tight relationship between organism form and function: a succulent, long-lived, photosynthetic stem allows cacti to survive long periods of drought while maintaining a positive tissue water status. Pereskia (Cactaceae) comprises 17 species of leafy shrubs and trees that are thought to represent the original cactus condition. Recent phylogenetic work has shown that there are two separate clades of Pereskia species, which are basal and paraphyletic with respect to the rest of the cacti. We selected seven Pereskia species, representing both clades, and characterized their water relations by measuring a suite of physiological traits in wild populations. Additionally, we estimated basic climate parameters from collection localities for all 17 Pereskia species. Extant Pereskia species exhibit ecological water use patterns that are very similar to those of the leafless, stem-succulent cacti. Ancestral trait reconstruction for the physiological and environmental data provides a preliminary assessment of the ecology and water relations of the earliest cacti and suggests that several key elements of the cactus ecological niche were established before the evolution of the cactus life-form. We interpret these ecological traits as potentially important drivers of evolutionary innovation in the cacti.     

Basal cactus phylogeny: implications of Pereskia (Cactaceae) paraphyly for the transition to the cactus life form

The cacti are well-known desert plants, widely recognized by their specialized growth form and essentially leafless condition. Pereskia, a group of 17 species with regular leaf development and function, is generally viewed as representing the "ancestral cactus," although its placement within Cactaceae has remained uncertain. Here we present a new hypothesis of phylogenetic relationships at the base of the Cactaceae, inferred from DNA sequence data from five gene regions representing all three plant genomes. Our data support a basal split in Cactaceae between a clade of eight Pereskia species, centered around the Caribbean basin, and all other cacti. Two other Pereskia clades, distributed mostly in the southern half of South America, are part of a major clade comprising Maihuenia plus Cactoideae, and Opuntioideae. This result highlights several events in the early evolution of the cacti. First, during the transition to stem-based photosynthesis, the evolution of stem stomata and delayed bark formation preceded the evolution of the stem cortex into a specialized photosynthetic tissue system. Second, the basal split in cacti separates a northern from an initially southern cactus clade, and the major cactus lineages probably originated in southern or west-central South America.     

Correlated evolution of stem and leaf hydraulic traits in Pereskia (Cactaceae)

Recent studies have demonstrated significant correlations between stem and leaf hydraulic properties when comparing across species within ecological communities. This implies that these traits are co-evolving, but there have been few studies addressing plant water relations within an explicitly evolutionary framework. This study tests for correlated evolution among a suite of plant water-use traits and environmental parameters in seven species of Pereskia (Cactaceae), using phylogenetically independent contrasts. There were significant evolutionary correlations between leaf-specific xylem hydraulic conductivity, Huber Value, leaf stomatal pore index, leaf venation density and leaf size, but none of these traits appeared to be correlated with environmental water availability; only two water relations traits - mid-day leaf water potentials and photosynthetic water use efficiency - correlated with estimates of moisture regime. In Pereskia, it appears that many stem and leaf hydraulic properties thought to be critical to whole-plant water use have not evolved in response to habitat shifts in water availability. This may be because of the extremely conservative stomatal behavior and particular rooting strategy demonstrated by all Pereskia species investigated. These results highlight the need for a lineage-based approach to understand the relative roles of functional traits in ecological adaptation.     

The closest relatives of cacti: insights from phylogenetic analyses of chloroplast and mitochondrial sequences with special emphasis on relationships in the tribe Anacampseroteae

Recent molecular and morphological systematic investigations revealed that the cacti are most closely related to Anacampseroteae, Portulaca and Talinum of the family Portulacaceae (ACPT clade of suborder Portulacineae). A combined analysis of ndhF, matK, and nad1 sequence data from the chloroplast and the mitochondrial genomes indicates that the tribe Anacampseroteae is the sister group of the family Cactaceae. This clade, together with Portulaca, is well characterized by the presence of axillary hairs or scales. Relationships within Anacampseroteae are characterized by a grade of five species of Grahamia s.l. from North and South America, and Grahamia australiana is found to be sister to the genera Anacampseros and Avonia. A comparison of vegetative characteristics indicates an evolutionary transition from woody subshrubs to dwarf perennial and highly succulent herbs during the diversification of Anacampseroteae. Available evidence from the present investigation as well as from previously published studies suggests that a revised classification of Portulacineae on the basis of inferred phylogenetic relationships might consist of a superfamily that includes Cactaceae and the three genera Anacampseros s.l. (including Avonia and Grahamia s.l.), Portulaca, and Talinum (including Talinella), either referred to three monogeneric families or to a paraphyletic family Portulacaceae*.     

Ecological physiology of Pereskia guamacho, a cactus with leaves

The specialized physiology of leafless, stem-succulent cacti is relatively well understood. This is not true, however, for Pereskia (Cactaceae), the 17 species of leafy trees and shrubs that represent the earliest diverging lineages of the cacti. Here we report on the water relations and photosynthesis of Pereskia guamacho, a small tree of the semiarid scrubland of Venezuela's Caribbean coast. Sapwood-specific xylem conductivity (Ksp) is low when compared to other vessel-bearing trees of tropical dry systems, but leaf-specific xylem conductivity is relatively high due to the high Huber value afforded by P. guamacho's short shoot architecture. P. guamacho xylem is not particularly vulnerable to drought-induced cavitation, especially considering the high leaf water potentials maintained year round. This is confirmed by the lack of significant variation exhibited in Ksp between wet and dry seasons. In the rainy season, P. guamacho exhibited C3-like patterns of stomatal conductance, but during a prolonged drought we documented nocturnal stomatal opening with a concomitant accumulation of titratable acid in leaves. This suggests that P. guamacho can perform drought-induced crassulacean acid metabolism (CAM photosynthesis), although delta 13C values imply that most carbon is assimilated via the C3 pathway. P. guamacho leaves display very low stomatal densities, and maximum stomatal conductance is low whether stomata open during the day or night. We conclude that leaf performance is not limited by stem hydraulic capacity in this species, and that water use is conservative and tightly regulated at the leaf level.     

Phylogenetic relationships in the cactus family (Cactaceae) based on evidence from trnK/ matK and trnL-trnF sequences

Cacti are a large and diverse group of stem succulents predominantly occurring in warm and arid North and South America. Chloroplast DNA sequences of the trnK intron, including the matK gene, were sequenced for 70 ingroup taxa and two outgroups from the Portulacaceae. In order to improve resolution in three major groups of Cactoideae, trnL-trnF sequences from members of these clades were added to a combined analysis. The three exemplars of Pereskia did not form a monophyletic group but a basal grade. The well-supported subfamilies Cactoideae and Opuntioideae and the genus Maihuenia formed a weakly supported clade sister to Pereskia. The parsimony analysis supported a sister group relationship of Maihuenia and Opuntioideae, although the likelihood analysis did not. Blossfeldia, a monotypic genus of morphologically modified and ecologically specialized cacti, was identified as the sister group to all other Cactoideae. The tribe Cacteae was found to be sister to a largely unresolved clade comprising the genera Calymmanthium, Copiapoa, and Frailea, as well as two large and well-supported clades. Browningia sensu stricto (excluding Castellanosia), the two tribes Cereeae and Trichocereeae, and parts of the tribes Notocacteae and Rhipsalideae formed one clade. The distribution of this group is largely restricted to South America. The other clade consists of the columnar cacti of Notocacteae, various genera of Browningieae, Echinocereeae, and Leptocereeae, the tribes Hylocereeae and Pachycereeae, and Pfeiffera. A large portion of this latter group occurs in Central and North America and the Caribbean.     

Wide-band tracheids are present in almost all species of Cactaceae

Wide-band tracheids (WBTs) have been found in seedlings of most species of cacti that have fibrous wood in their adult bodies. Consequently, this cell type is now known to be present in almost all cacti. Earlier studies of adult plants revealed WBTs to be present only in cacti with globose or short, broad bodies, whereas all species with large columnar or long slender bodies had fibrous wood without WBTs. However, even these species produce WBTs during the first several months after germination. In species with fibrous wood in their adult bodies (species with large or slender bodies), seedlings undergo a phase transition in wood morphogenesis after a few months and stop producing the juvenile (WBT) wood and begin producing adult (fibrous) wood. If adult plants have an intermediate size, the phase transition is delayed and the plant produces WBT wood for several years. Species with globose bodies repress the phase transition completely and never switch to producing adult (fibrous) wood. Because WBTs are so widespread, they probably originated only once in Cactaceae, not multiple times as suggested earlier, or there may have been just a single origin in the Cactaceae/Portulacaceae clade.     

Characterization and Partial Purification of Aldose-6-phosphate Reductase (Alditol-6-Phosphate:NADP 1-Oxidoreductase) from Apple Leaves

The Pereskia are morphologically primitive, leafed members of the Cactaceae. Gas exchange characteristics using a dual isotope porometer to monitor ¹⁴CO₂ and tritiated water uptake, diurnal malic acid fluctuations, phosphoenolpyruvate carboxylase, and malate dehydrogenase activities were examined in two species of the genus Pereskia, Pereskia grandifolia and Pereskia aculeata. Investigations were done on well watered (control) and water-stressed plants. Nonstressed plants showed a CO₂ uptake pattern indicating C₃ carbon metabolism. However, diurnal fluctuations in titratable acidity were observed similar to Crassulacean acid metabolism. Plants exposed to 10 days of water stress exhibited stomatal opening only during an early morning period. Titratable acidity, phosphoenolpyruvate carboxylase activity, and malate dehydrogenase activity fluctuations were magnified in the stressed plants, but showed the same diurnal pattern as controls. Water stress causes these cacti to shift to an internal CO₂ recycling (“idling”) that has all attributes of Crassulacean acid metabolism except nocturnal stomata opening and CO₂ uptake. The consequences of this shift, which has been observed in other succulents, are unknown, and some possibilities are suggested.     

Evolution of extreme xeromorphic characters in wood: a study of nine evolutionary lines in Cactaceae

Vessels of xeric-adapted woods have been predicted to be narrower than those of mesic-adapted woods, to occur at higher densities, to occur in larger clusters, and to have a greater percentage of them in clusters. These predictions were tested by comparing wood structure of several evolutionary lines of xeric-adapted cacti to that of mesic-adapted Pereskia, which probably resembles the ancestral cacti. Although derived cacti occur in habitats with water stress ranging from mild (rain forests) to severe (open deserts with little vegetation other than cacti), as long as plants retain wood with an ordinary fibrous matrix, wood characters are remarkably uniform and not correlated with habitat aridity. However, in several evolutionary lines, novel wood types occur with characters that fulfill the predictions for xeric-adapted woods listed above. However, conductive area (fraction of wood transverse-sectional area occupied by conduits) and estimated specific conductance (conductance per square millimetre) are correlated with shoot height (the need for mechanical support from xylary fibers) rather than with habitat aridity: tall plants transport water through relatively few, wide vessels, permitting much of the wood volume to consist of fibers. Small plants with little wood use large numbers of narrow vessels rather than small numbers of wide ones, thereby achieving conductive safety.     

Molecular phylogeny of Nyctaginaceae: taxonomy, biogeography, and characters associated with a radiation of xerophytic genera in North America

The four o'clock family (Nyctaginaceae) has a number of genera with unusual morphological and ecological characters, several of which appear to have a "tendency" to evolve repeatedly in Nyctaginaceae. Despite this, the Nyctaginaceae have attracted little attention from botanists. To produce a phylogeny for the Nyctaginaceae, we sampled 51 species representing 25 genera (of 28-31) for three chloroplast loci (ndhF, rps16, rpl16, and nrITS) and included all genera from North America. Parsimony, likelihood, and Bayesian methods were used to reconstruct the phylogeny for the family. The family is neotropical in origin. A radiation of woody taxa unites Pisonia and Pisoniella with the difficult tropical genera Neea and Guapira, which also form a clade, though neither appears to be monophyletic. This group is sister to a clade containing Bougainvillea, Belemia, and Phaeoptilum. A dramatic radiation of genera occurred in the deserts of North America. The tribe Nyctagineae and its subtribes are paraphyletic, due to over-reliance on a few homoplasious characters, i.e., pollen morphology and involucre presence. Two notable characters associated with the desert radiation are cleistogamy and edaphic endemism on gypsum soils. We discuss evolutionary trends in these traits in light of available data about self-incompatibility and gypsum tolerance in Nyctaginaceae.     

The position of Cetacea within mammalia: phylogenetic analysis of morphological data from extinct and extant taxa

Knowledge of the phylogenetic position of the order Cetacea (whales, dolphins, and porpoises) within Mammalia is of central importance to evolutionary biologists studying the transformations of biological form and function that accompanied the shift from fully terrestrial to fully aquatic life in this clade. Phylogenies based on molecular data and those based on morphological data both place cetaceans among ungulates but are incongruent in other respects. Morphologists argue that cetaceans are most closely related to mesonychians, an extinct group of terrestrial ungulates. They have disagreed, however, as to whether Perissodactyla (odd-toed ungulates) or Artiodactyla (even-toed ungulates) is the extant clade most closely related to Cetacea, and have long maintained that each of these orders is monophyletic. The great majority of molecule-based phylogenies show, by contrast, not only that artiodactyls are the closest extant relatives of Cetacea, but also that Artiodactyla is paraphyletic unless cetaceans are nested within it, often as the sister group of hippopotamids. We tested morphological evidence for several hypotheses concerning the sister taxon relationships of Cetacea in a maximum parsimony analysis of 123 morphological characters from 10 extant and 30 extinct taxa. We advocate treating certain multistate characters as ordered because such a procedure incorporates information about hierarchical morphological transformation. In all most-parsimonious trees, whether multistate characters are ordered or unordered, Artiodactyla is the extant sister taxon of Cetacea. With certain multistate characters ordered, the extinct clade Mesonychia (Mesonychidae + Hapalodectidae) is the sister taxon of Cetacea, and Artiodactyla is monophyletic. When all fossils are removed from the analysis, Artiodactyla is paraphyletic with Cetacea nested inside, indicating that inclusion of mesonychians and other extinct stem taxa in a phylogenetic analysis of the ungulate clade is integral to the recovery of artiodactyl monophyly. Phylogenies derived from molecular data alone may risk recovering inconsistent branches because of an inability to sample extinct clades, which by a conservative estimate, amount to 89% of the ingroup. Addition of data from recently described astragali attributed to cetaceans does not overturn artiodactyl monophyly.     

Stem tilting in the inter‐tropical cactus Echinocactus platyacanthus: an adaptive solution to the trade‐off between radiation acquisition and temperature control

While plants require radiation for photosynthesis, radiation in warm deserts can have detrimental effects from high temperatures. This dilemma may be solved through plant morphological attributes. In cold deserts, stem tilting keeps reproductive organs warm by increasing radiation interception at the cost of decreased annual light interception. Conversely, little is known about stem tilting in warm deserts. We hypothesised that stem tilting in Echinocactus platyacanthus prevents high temperatures near the apex, where reproduction occurs. The study was conducted in the warm, inter‐tropical portion of the Chihuahuan Desert, Mexico. We found that cacti preferentially tilted towards the south, which reduced temperatures of reproductive organs during the hot season, but increased total annual near‐apex PAR interception. Tilting also maximised reproduction, a likely consequence of temperature control but perhaps also of the difficulty in translocating photosynthates in cacti; therefore, annual energy acquisition near floral meristems may be largely allocated to reproduction. Unlike plants of higher latitudes, in inter‐tropical deserts sunlight at noon comes either from the north or the south, depending on the season, and thus stem tilting may more strongly affect total annual radiation received in different portions of the stem. Inter‐tropical cacti can synchronise reproduction with irradiance peaks if flowering occurs in a specific (north or south) portion of the stem; also, they effectively solve the conflict between maximising annual PAR interception and minimising temperature at the hottest time of day. Notably, the two inter‐tropical cacti in which stem tilting has been studied successfully solve this conflict.     

Phylogenetic relationships of Rhododendroideae (Ericaceae)

The Rhododendroideae are usually recognized as a subfamily within Ericaceae. This group has been considered primitive (i.e., occupying the ancestral or basal position relative to all other Ericaceae) due to the occurrence of separate petals in several taxa, deciduous corollas, and septicidally dehiscent capsules. Previous molecular studies using rbcL and nr18s sequences have indicated that Rhododendroideae may be paraphyletic and cladistically derived (i.e., the relative position in the geneology of Ericaceae is not basal). The matK sequences of 42 taxa from traditional Rhododendroideae and potentially related clades were obtained via standard gene amplication and double-stranded dideoxy sequencing. Phylogenetic analyses of these sequences using Actinidia chinensis as the outgroup indicate that the Rhododendroideae are paraphyletic. Trees obtained in the analyses indicate an expanded rhododendroid clade that includes four major subclades - empetroid, rhodo, ericoid, and phyllodocoid. The ericoid clade is sister to the phyllodocoid clade and the empetroid clade is sister to the rhodo clade. Relationships within the clades are generally well resolved except within the rhodo clade where matK data indicate that Rhododendron is probably paraphyletic. Daboecia and Calluna are included within the ericoid clade; Erica is paraphyletic. Cassiope lies outside the rhododendroid clade. The relationships indicated by the matK data suggest that sympetalous flowers are likely plesiomorphic within rhododendroids.     

Molecular phylogenetics of suborder Cactineae (Caryophyllales), including insights into photosynthetic diversification and historical biogeography

? Premise of the study: Phylogenetic relationships were investigated among the eight families (Anacampserotaceae, Basellaceae, Cactaceae, Didiereaceae, Halophytaceae, Montiaceae, Portulacaceae, Talinaceae) that form suborder Cactineae (= Portulacineae) of the Caryophyllales. In addition, photosynthesis diversification and historical biogeography were addressed. ? Methods: Chloroplast DNA sequences, mostly noncoding, were used to estimate the phylogeny. Divergence times were calibrated using two Hawaiian Portulaca species, due to the lack of an unequivocal fossil record for Cactineae. Photosynthetic pathways were determined from carbon isotope ratios (δ(13)C) and leaf anatomy. ? Key results: Maximum likelihood and Bayesian analyses were consistent with previous studies in that the suborder, almost all families, and the ACPT clade (Anacampserotaceae, Cactaceae, Portulacaceae, Talinaceae) were strongly supported as monophyletic; however, relationships among families remain uncertain. The age of Cactineae was estimated to be 18.8 Myr. Leaf anatomy and δ(13)C and were congruent in most cases, and inconsistencies between these pointed to photosynthetic intermediates. Reconstruction of photosynthesis diversification showed C(3) to be the ancestral pathway, a shift to C(4) in Portulacaceae, and five independent origins of Crassulacean acid metabolism (CAM). Cactineae were inferred to have originated in the New World. ? Conclusions: Although the C(3) pathway is inferred as the ancestral state in Cactineae, some CAM activity has been reported in the literature in almost every family of the suborder, leaving open the possibility that CAM may have one origin in the group. Incongruence among loci could be due to internal short branches, which possibly represent rapid radiations in response to increasing aridity in the Miocene.     

A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): evolution of life-history traits and host switches

Phylogenetic analysis of genomic data allows insights into the evolutionary history of pathogens, especially the events leading to host switching and diversification, as well as alterations of the life cycle (life-history traits). Hundreds, perhaps thousands, of malaria parasite species exploit squamate reptiles, birds, and mammals as vertebrate hosts as well as many genera of dipteran vectors, but the evolutionary and ecological events that led to this diversification and success remain unresolved. For a century, systematic parasitologists classified malaria parasites into genera based on morphology, life cycle, and vertebrate and insect host taxa. Molecular systematic studies based on single genes challenged the phylogenetic significance of these characters, but several significant nodes were not well supported. We recovered the first well resolved large phylogeny of Plasmodium and related haemosporidian parasites using sequence data for four genes from the parasites' three genomes by combining all data, correcting for variable rates of substitution by gene and site, and using both Bayesian and maximum parsimony analyses. Major clades are associated with vector shifts into different dipteran families, with other characters used in traditional parasitological studies, such as morphology and life-history traits, having variable phylogenetic significance. The common parasites of birds now placed into the genus Haemoproteus are found in two divergent clades, and the genus Plasmodium is paraphyletic with respect to Hepatocystis, a group of species with very different life history and morphology. The Plasmodium of mammal hosts form a well supported clade (including Plasmodium falciparum, the most important human malaria parasite), and this clade is associated with specialization to Anopheles mosquito vectors. The Plasmodium of birds and squamate reptiles all fall within a single clade, with evidence for repeated switching between birds and squamate hosts.     

Wood Chemical Composition in Species of Cactaceae: The Relationship between Lignification and Stem Morphology

In Cactaceae, wood anatomy is related to stem morphology in terms of the conferred support. In species of cacti with dimorphic wood, a unique process occurs in which the cambium stops producing wide-band tracheids (WBTs) and produces fibers; this is associated with the aging of individuals and increases in size. Stem support and lignification have only been studied in fibrous tree-like species, and studies in species with WBTs or dimorphic wood are lacking. In this study, we approach this process with a chemical focus, emphasizing the role of wood lignification. We hypothesized that the degree of wood lignification in Cactaceae increases with height of the species and that its chemical composition varies with wood anatomy. To test this, we studied the chemical composition (cellulose, hemicellulose, and lignin content) in 13 species (2 WBTs wood, 3 dimorphic, and 8 fibrous) with contrasting growth forms. We also analyzed lignification in dimorphic and fibrous species to determine the chemical features of WBTs and fibers and their relationship with stem support. The lignin contents were characterized by Fourier transform infrared spectroscopy and high performance liquid chromatography. We found that 11 species have a higher percentage (>35%) of lignin in their wood than other angiosperms or gymnosperms. The lignin chemical composition in fibrous species is similar to that of other dicots, but it is markedly heterogeneous in non-fibrous species where WBTs are abundant. The lignification in WBTs is associated with the resistance to high water pressure within cells rather than the contribution to mechanical support. Dimorphic wood species are usually richer in syringyl lignin, and tree-like species with lignified rays have more guaiacyl lignin. The results suggest that wood anatomy and lignin distribution play an important role in the chemical composition of wood, and further research is needed at the cellular level.     

Giant Tortoises as Ecological Engineers: A Long-term Quasi-experiment in the Galápagos Islands

Giant tortoises were once a megafaunal element widespread in tropical and subtropical ecosystems. The role of giant tortoises as herbivores and seed dispersers, however, is poorly known. We evaluated tortoise impacts on Opuntia cactus (Cactaceae) in the Galápagos Islands, one of the last areas where giant tortoises remain extant, where the cactus is a keystone resource for many animals. We contrasted cactus populations immediately inside and outside natural habitats where tortoises had been held captive for several decades. Through browsing primarily and trampling secondarily tortoises strongly reduced densities of small (0.5–1.5 m high) cacti, especially near adult cacti, and thereby reduced densities of cacti in larger size classes. Tortoises also caused a shift from vegetative to sexual modes of reproduction in cacti. We conclude that giant tortoises promote a sparse and scattered distribution in Opuntia cactus and its associated biota in the Galápagos Islands.     

A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences

A phylogeny of haemosporidian parasites (phylum Apicomplexa, family Plasmodiidae) was recovered using mitochondrial cytochrome b gene sequences from 52 species in 4 genera (Plasmodium, Hepatocystis, Haemoproteus, and Leucocytozoon), including parasite species infecting mammals, birds, and reptiles from over a wide geographic range. Leucocytozoon species emerged as an appropriate out-group for the other malarial parasites. Both parsimony and maximum-likelihood analyses produced similar phylogenetic trees. Life-history traits and parasite morphology, traditionally used as taxonomic characters, are largely phylogenetically uninformative. The Plasmodium and Hepatocystis species of mammalian hosts form 1 well-supported clade, and the Plasmodium and Haemoproteus species of birds and lizards form a second. Within this second clade, the relationships between taxa are more complex. Although jackknife support is weak, the Plasmodium of birds may form 1 clade and the Haemoproteus of birds another clade, but the parasites of lizards fall into several clusters, suggesting a more ancient and complex evolutionary history. The parasites currently placed within the genus Haemoproteus may not be monophyletic. Plasmodium falciparum of humans was not derived from an avian malarial ancestor and, except for its close sister species, P. reichenowi, is only distantly related to haemospordian parasites of all other mammals. Plasmodium is paraphyletic with respect to 2 other genera of malarial parasites, Haemoproteus and Hepatocystis. Explicit hypothesis testing supported these conclusions.