Evolution And Systematics

Robert S. Wallace and Arthur C. Gibson

Introduction

Phylogenetic Placement of Cactaceae

Cactaceae, a Family of Order Caryophyllales Classification of Cactaceae within Suborder Portulacineae Cactaceae, a Monophyletic Family Defining Subfamilies of Cactaceae

Transitions from Structural Analyses to Molecular Systematics Molecular Systematics of Cactoideae Identifying the Oldest Taxa Epiphytic Cacti Columnar Cactus Lineages Cacteae and Notocacteae

Solving Classification Problems Using Molecular Techniques Phylogenetic Studies of Subfamily Opuntioideae New Insights into Cactus Evolution Structural Properties

Revised Biogeographic Models Based on Molecular Studies Concluding Remarks Literature Cited

Introduction

The Cactaceae is one of the most popular, easily recognizable, and morphologically distinct families of plants, and it includes approximately 1,600 species (Gibson and Nobel 1986; Barthlott and Hunt 1993). Cacti occur in the New World from western and southern Canada (Speirs 1982) to southern Patagonia in Chile and Argentina (Kiesling 1988), and the epiphytic genus Rhipsalis has dispersed naturally, undoubtedly by birds, to tropical Africa and Madagascar and across to Sri Lanka and southern India (Thorne

1973; Barthlott 1983). These usually spiny organisms (Fig. 1.1) are loved by plant fanciers for their diverse forms and showy flowers. Nearly every introductory college biology or ecology textbook contains at least one cactus photograph, used to illustrate plant adaptation to dry habitats. Important commercial products are derived from cacti (Nobel 1994, 1998). Cacti have also helped evolutionary biologists and ecologists understand CAM (Crassulacean acid metabolism) and succulence (Gibson and Nobel 1986; Nobel 1988, 1991).

In some plant families, it is merely a matter of con

Figure i.i. The vegetative plant of Coryphantha bumamma (Ehrenberg) Brittton and Rose (tribe Cacteae), a low-growing spherical cactus from Guerrero, Mexico.

venience to have correct names for plant species. In the Cactaceae, however, there is not only a huge demand for correct names and precise classification into genera, but also a critical need for a phylogenetic classification because there are many subjects, some of which are covered in this book, that depend on having an accurate evolutionary reconstruction of cactus history.

Phylogenetic Placement of Cactaceae

Cactaceae, a Family of Order Caryophyllales

Family Cactaceae is assigned to order Caryophyllales, which includes, among others, ice plants (Aizoaceae), portulacas (Portulacaceae), carnations (Caryophyllaceae), bougainvilleas (Nyctaginaceae), pokeweeds (Phytolac-caceae), amaranths (Amaranthaceae), and saltbushes (Chenopodiaceae). The taxonomic history of classifying Cactaceae within this order has been adequately reviewed (Cronquist and Thorne 1994), and there is universal acceptance that cacti are core members of Caryophyllales.

Phylogenetic placement within the Caryophyllales is undisputed, because cacti and other families within the order share derived characters, i.e., synapomorphies, that do not occur in any other angiospermous order. One structural synapomorphy, and the first recognized feature for relating these families, is that the seed contains a strongly curved, peripheral embryo around a central nutritive perisperm, not endosperm. From that observation arose the ordinal name Centrospermae (Eichler 1878). A chemical synapomorphy is the occurrence of betalains, a class of nitrogenous pigments derived from tyrosine (Mabry 1964; Clements et al. 1994). The Cactaceae and closely related families form a proteinaceous plastid inclusion (designated as type P3cf) during the ontogeny of sieve-tube members (Behnke i976a,b, 1994). Congruence of the three mentioned unlinked and unique synapomorphic characters in these same families, not in others, formed a solid case for recognizing this monophyletic clade.

Order Caryophyllales, which was established by analyzing certain types of structural and chemical data, was tested with a new data set using chloroplast DNA (cpDNA) restriction site mutations, and was confirmed by the loss of the rph intron in the common ancestor of the order (Downie and Palmer 1994). Indeed, investigators use whatever data are available at the time to formulate an initial hypothesis, and later test the model using an indisputable data set of a totally different nature that provides resolution. Yet there are still some unresolved issues concerning the composition of Caryophyllales and whether other families, shown by molecular studies to share closest DNA affinities to Caryophyllales, should be classified within the order (Angiosperm Phylogeny Group 1998). Among these are the insectivorous sundews (Droseraceae) and pitcher plants of Nepenthaceae. It is unclear at this time whether molecular data will require these nontradi-tional members to be classified within the order or instead as allies in one or more separate orders. Regardless of that outcome, placement of family Cactaceae is unaffected for the time being.

Classification of Cactaceae within Suborder Portulacineae

Phylogenetic relationships of the Cactaceae within the Caryophyllales have been much more difficult to determine. Investigators have been interested in determining to which of the betalain-containing families Cactaceae is phy-logenetically most closely related. Traditional comparative and developmental evidence favored the Aizoaceae (Turner 1973; Rodman et al. 1984) or Phytolaccaceae (Buxbaum 1953; Cronquist 1981), emphasizing floral features. More recent analyses claimed that the Cactaceae has most recent ancestry with the Portulacaceae (Thorne 1983; Gibson and Nobel 1986; Hershkovitz 1991; Gibson 1994), within what became called suborder Portulacineae Thorne (Cronquist and Thorne 1994), which included Cactaceae, Portula-caceae, Didiereaceae, and Basellaceae.

New data sets from gene sequence experiments tested the model and strongly supported Portulacineae as a monophyletic taxon that includes Cactaceae (Manhart and Rettig 1994). Cactaceae and certain Portulacaceae are sister taxa sharing a 500 base-pair (bp) deletion in the Rubisco gene rbcL (Rettig et al. 1992; Downie and Palmer 1994). Using a 1,100 bp sequence of open reading frame in cpDNA, the largest gene in the chloroplast genome, Downie et al. (1997) concluded again that Pereskia (Cactaceae) belongs in the portulacaceous cohort. With internal transcribed spacer sequences of cpDNA, Hershkovitz and Zimmer (1997) obtained results that placed the primitive leaf-bearing cacti phylogenetically nested within the Portulacaceae, and the Cactaceae was identified as the sister taxon of a clade that includes species of Talinum. In a more intensive cpDNA analysis of the portulacaceous cohort, using gene sequence data of ndhF, a recent study has shown that the Cactaceae is indeed nested within the Portulacaceae sensu lato and is most closely related to

Talinum and Portulaca (Fig. 1.2; Appleqvist and Wallace 2001). In future systematic studies of the family, these sequence data will play an important role in redefining the family Portulacaceae, as well as the evolutionarily distinct groups it now contains, and how the evolutionary components of this diverse clade need to be circumscribe®

Cactaceae, a Monophyletic Family

Even casual students of cacti can recognize the repetitive vegetative design within this plant family (Gibson and Nobel 1986). Typically, a cactus possesses a perennial pho-tosynthetic succulent stem, bearing leaf spines produced on modified axillary buds, termed areoles, but lacking broad green leaves. The colorful flower of the typical cactus has many separate perianth parts, numerous stamens, and an inferior ovary with many ovules and parietal placentation. The fruit is a many-seeded berry, often juicy but in some taxa becoming dry or splitting open at maturity. There are, of course, exceptional forms: (1) spineless plants (e.g., certain epiphytes such as Disocactus and Epiphyllum and small cacti such as Lophophora and Ariocarpus); (2) geophytes with annual above-ground shoots (e.g., Pterocactus kuntzei, Opuntia chaffeyi, and Peniocereus striatus); (3) primitive cacti that have relatively broad, dorsiventrally flattened leaves (e.g., Pereskia spp. and Pereskiopsisporteri); (4) plants that have relatively small flowers with fewer parts (e.g., small-flowered species of Rhipsalis, Pseudorhipsalis, and Uebelmannia spp.); and (5) superior ovaries with axile placentation (e.g., Pereskia sacharosa). None of these exceptions is troubling, because all are well-accepted members of the family and understood as representing either primitive or highly reduced, apomorphic (derived) states of cactus features.

The morphological distinctiveness and monophyly of family Cactaceae have been further supported conclusively with molecular data. There has occurred a 6 kb inversion in the large single copy region of the plastid genome (relative to the consensus land plant gene order seen in Nicotiana tabacum; Downie and Palmer 1993) that involves the genes atpE, atpB, and rbcL. This cpDNA inversion has been found in all cacti sampled, so this is an excellent molecular synapomorphy for defining Cactaceae (Wallace 1995; Wallace and Forquer 1995; Wallace and Cota 1996; Cota and Wallace 1996, 1997). Remarkably, an identical inversion of the same cpDNA region occurs independently in another caryophyllalean lineage, the Chenopodiaceae (Downie and Palmer 1993). Nonetheless, because cacti consistently exhibit this 6 kb inversion, molecular system-atists infer that Cactaceae are monophyletic, i.e., traceable back to a single ancestral population in which the inversion appeared and then became genetically fixed. What remains

Amaranthus palmeri A. quitensis Mollugo verticillata Allionia violacea Mirabilisjalapa Bougainvillea sp. Phytolacca acinosa Aptenia cordifolia Tetragonia tetragonioides Talinum paniculatum T. angustissimum T. caffrum T. triangulare Talinella pachypoda Anacampseros retusa Grahamia bracteata Talinopsis frutescens Portulaca grandiflora P. mundula P. molokiniensis P. oleracea Maihuenia poeppigii Pereskia aculeata Quiabentia verticillata Montia perfoliata Claytonia virginica Montia diffusa M. parvifola Lewisia pygmaea Calandrinia volubilis C. ciliata var. menziesii C. compressa Montiopsis umbellata M. berteroana M. cumingii Cistanthe grandiflora C. mucronulata C. guadalupensis Calyptridium umbellatum Talinum mengesii Alluaudia humbertii Didierea trollii Calyptrotheca somalensis Ceraria fruticulosa Portulacaria afra Basella alba Ullucus tuberosus

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