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Repeated Evolution of Succulent Haseltonia.14:.26–36..2008. 26 . HASELTONIA 14,.2008. 27 VARIATIONS ON A THEME: REPEATED lineages of succulent life forms emerging from eage comprises about 2200 species, of which what was once recognized as the family Portu- about 90% are classified as succulents (Eggli EVOLUTION OF SUccULENT LIFE FORMS IN THE lacaceae (Hershkovitz and Zimmer 1997; Ap- 2002; Anderson 2005; Hunt 2006). Relation- PORTULACINEAE (CARYOPHYLLALES) plequist and Wallace 2001; Nyffeler 2007). In ships among the members of suborder Portu- addition to the cacti, there has been the evo- lacineae have recently been further clarified Reto Nyffeler lution of (1) perennial rosette-forming herbs (Nyffeler 2007). The family Portulaceae s.l. is with persistent succulent leaves (such as Lew- found to be paraphyletic; some of its species Institut für Systematische Botanik, Universität Zürich, isia in western North America; Fig 2), (2) pe- are more closely related to either Cactaceae or Zollikerstrasse 107, CH-8008 Zürich, Switzerland rennial herbs with fleshy roots and highly suc- Didiereaceae rather than to some other spe- culent or greatly reduced leaves (Anacampseros cies of the same family (Fig 13). Urs Eggli and Avonia; Figs 3, 4), (3) annual herbs with The genera Ceraria and Portulacaria are Sukkulenten-Sammlung Zürich, Mythenquai 88, CH-8002 Zürich, Switzerland prostrate, fleshy stems and succulent leaves most closely related to traditional Didierea- (including Portulaca oleracea, P. afra, and their ceae, while the genera Anacampseros, Avonia, Matt Ogburn & Erika Edwards relatives; Figs 5, 6), (4) small, pachycaulescent Grahamia s. l. (including Talinaria, Talinopsis, Department of Ecology and Evolutionary Biology, Brown shrubs or trees with succulent leaves (Ceraria and Xenia—in composite referred to as tribe University, 80 Waterman St, Providence, RI 02912, USA from southern Africa; Fig 7) and long shoot– Anacampseroteae; Rowley 1994, 1995), as short shoot differentiation (Didierea in Mad- well as Portulaca and Talinum (the latter in a agascar; Fig 8), (5) subwoody shrubs with tu- revised circumscription excluding the mem- berous roots and herbaceous leaves (Talinum bers of the former section Phemeranthus but paniculatum and relatives; Figs 9–11), and (6) including the Madagascan endemic genus Abstract: The succulent life form is a tried and true strategy for plants living in arid envi- slightly succulent scramblers or vines with a Talinella), form a well supported clade to- ronments. It has evolved in many distantly related lineages comprising 12,500 species from thickened stem base (such as Basella and re- gether with the family Cactaceae. This clade 70 flowering plant families and has spawned remarkable radiations. Three major groups are lated genera mainly from the tropics of the was referred to as the “ACPT clade” (that is, generally recognized: (1) stem succulents (that is, leafless cactus-like growth forms), (2) leaf New World; Fig 12). Anacampseroteae, Cactaceae, Portulaca, Tali- succulents, and (3) caudiciform and pachycaul succulents. All three lifeform groups are rep- This new phylogenetic picture allows us to num) by Nyffeler (2007). These findings re- resented in the relatively small suborder Portulacineae. Here we suggest that this diversity place the evolution of Cactaceae within a richer ceive good statistical support from molecular provides a unique opportunity to evaluate early cactus evolution within a richer contextual context and ask the following questions: (1) sequences of the chloroplast genome. Further- framework. We briefly review what we know about the phylogenetic relationships within the What do the cacti have in common with their more, morphological and anatomical charac- suborder Portulacineae (that is, Basellaceae, Cactaceae, Didiereaceae, and Portulacaceae) and other succulent relatives, and how do they dif- teristics provide additional evidence in favor the morphology and ecology of all major Portulacineae lineages. We then outline what we fer? (2) What did the ancestral Portulacineae of these inferred relationships (Ogburn 2007; believe to be key areas for future research on these understudied plants and discuss several look like, and where did it arise? (3) Can we Nyffeler and Eggli submitted). hypothetical “pre-adaptations” and conditions in ancestral Portulacineae that may have pro- infer the ecological conditions that may have Overall, we may recognize four major lin- moted the repeated evolution of unusual succulent life forms. triggered such dramatic morphological inno- eages in Portulacineae (Fig 13): (1) The resur- Key words: Caryophyllales, Portulacineae, Montiaceae, succulence, life form, functional vation in these lineages, and were they simi- rected family Montiaceae, here represented by trait, cactus, evolution lar in each case? (4) Can we infer anatomical the three genera Claytonia, Lewisia, and Phe- or functional pre-conditions that enable the meranthus, includes about 200 species mainly evolution of succulence? with herbaceous, rosettiform habits and clasp- Here we review what we currently know ing, non-constricted leaf bases. This family is Introduction Cactoideae and Opuntioideae is the result of about the evolutionary relationships, ecol- most prominent in the western parts of North Trained botanists and amateurs alike have re- the following modifications: (1) leaves highly ogy, and vegetative morphology of the Por- and South America. (2) The family Basella- garded the cacti with awe for centuries (Row- reduced, (2) short shoots (areoles) bear spines tulacineae and outline what we believe to be ceae forms a distinct and morphologically well ley 1997). The copious production of spines, derived from leaf primordia, (3) branching re- key areas for future research on these under- characterized clade of about 20 species that are lack of leaves, bizarre architecture due to the duced or absent, (4) long-lived stem epidermis studied plants. distributed in the tropics of the New World, formation of stem succulence, and the im- with delayed bark formation, and (5) cortex Africa, and Madagascar. (3) The family Didie- pressive ability to persist in warm arid des- and pith are expanded to form a water-stor- Phylogenetics of the reaceae is here used in the expanded circum- erts under some of the harshest environ- age tissue. Recent work on the phylogenetics suborder Portulacineae scription (Applequist and Wallace 2003) that mental conditions on Earth are all traits that of Pereskia (Edwards and others 2005; Butter- Today, the methods of molecular systematics includes Ceraria, Portulacaria, and possibly have entitled this lineage to be recognized as worth and Wallace 2005), as well as studies of allow us to reconstruct phylogenetic relation- also Calyptrotheca. These taxa generally form a prominent textbook example for adaptive Pereskia anatomy (Ogburn 2007), physiology, ships among groups of organisms in detail and large woody trees or shrubs, some with a dis- evolution in biology (for instance, Futuyma and ecology (Martin and Wallace 2000; Ed- with good measures of statistical support. Mo- tinct cactus-like habit, and occur in eastern 1997; Niklas 1997). Pereskia, a group of rel- wards 2006; Edwards and Donoghue 2006) lecular phylogenetic investigations of the past and southern Africa and Madagascar. (4) The atively non-succulent, leafy shrubs and small has revealed that this genus, indeed, has much decade (for instance, Hershkovitz and Zimmer ACPT clade consists of the family Cactaceae trees (Fig 1), has long been considered the to tell about early events in the evolution of 1997, 2000; Applequist and Wallace 2001; as well as three distinct subclades from the tra- “evolutionary link” between “ordinary” pe- the cactus life form (summarized in Edwards Cuénoud and others 2001) have clearly shown ditional family Portulacaceae. The genus Tali- rennial plants and leafless cacti (Rauh 1979; and Donoghue 2006). that the traditional families Basellaceae, Cac- num (including the genus Talinella, Nyffeler Gibson and Nobel 1986; Mauseth and Lan- Here we argue that there is even more to taceae, Didiereaceae, and Portulacaceae (that 2007) takes a cladistically basal position and drum 1997; but see Griffith 2004). The cac- gain by looking beyond Pereskia. It is now clear is, suborder Portulacineae) are closely related forms the sister group to a subclade consisting tus-form of representatives of the subfamilies that the cactus family is only one of several to each other. Overall, this evolutionary lin- of Anacampseroteae (Anacampseros, Avonia, and 28. NYffeler AND.OTHERS—EVolutIon of succulent lIfe froms . HASELTONIA 14,.2008. 29 Grahamia), Cactaceae, and Portulaca. This latter Distribution North, Central, and South Distribution North America (W half of the ground tuber, caudex or rhizome; leaves rosulate, group is well characterized by the presence of America, open areas, dry woodland to rocky continent only, SW Canada to NW Mexico), herbaceous, thin-textured to slightly succulent, axillary hairs or scales. The present hypothesis slopes. on rocks or gravel in usually open places. annually deciduous, flat to narrowly linear. (Fig 13; Nyffeler 2007) favors a sister-group re- Systematics and evolution Previously con- Systematics A genus of about 16 species Distribution North and Central Amer- lationship between Anacampseroteae and Cac- ceived as a subgenus of Talinum, but recent (Hershkovitz and Hogan 2002; Hershkovitz ica, northeast Asia (Mongolia, Siberia), usu- taceae, though this result only receives mod- molecular
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