Amer. J. Bot. 73(3): 387-397. 1986. CLADISTIC TESTS OF HYPOTHESES CONCERNING EVOLUTION OF XEROPHYTES AND MESOPHYTES WITHIN TILLANDSIA SUBG. PHYTARRHIZA (BROMELIACEAE)l AMY JEAN GILMARTIN AND GREGORY K. BROWN2 OwnbeyHerbarium and Departmentof Botany, WashingtonState University, Pullman, Washington99164, and 2Departmentof Botany, University of Wyoming, Laramie,Wyoming 82071 ABSTRACT TillandsiaL. Subg.Phytarrhiza (Visiani) Baker (Bromeliaceae) is a distinctivegroup of about 35 epiphytic species. These exhibit a range of habits from xeric to mesic. The evolutionary relationshipsof the contrastingadaptations need to be establishedhere as well as in the subfamily as a whole. Relations between the subgenus and other tillandsioids are problematicaland phylogeneticreconstruction of its member-specieswould be facilitated by identification of Phytarrhiza'srelative (sistertaxon) sharingthe same most recent common ancestorwith Phy- tarrhiza.This paperexamines the two most likely sistertaxa, Subg.Pseudo-Catopsis Baker and Subg.Diaphoranthema (Beer) Baker. Diaphoranthema is rejectedas sister taxon. The accepted evolutionarytree, rooted by Pseudo-Catopsis,indicates that most habitalevolutionary changes in Phytarrhizahave been between mesic and semi-mesic forms and from mesic to xeric forms. Methods developed for testing specificevolutionary hypotheses are broadlyapplicable. THERE IS CONSIDERABLEinterest in the direction ofxeric specializations of otherwise mesic taxa; of evolution of species within Phytarrhiza as for example, coreaceous, linear leafed species well as for the entire genus and subfamily be- of Lycium (Solanaceae). Such xeric adaptations cause of questions raised by Pittendrigh (1948), might seem to be difficult to reverse, i.e., un- Medina (1974), and Benzing and Renfrow likely to evolve to a more mesic state. Stebbins (1971 a, b), and discussed by Benzing, Givnish (1974) pointed out, however, that any belief and Bermudes (1985), and Gilmartin (1983), that xerophytes, in general, are irreversibly regarding relationships between mesic, tank specialized has no foundation in fact. We are forms and more strees-adapted "atmospheric left with both courses being essentially equally bromeliads." Benzing et al. (1985) examined probable. the question: are extreme xeric tillandsioids Geographic areas that might be paricularly derived from mesic forms- Schimper's (1888) prone to harbor evolutionary sequences of a interpretation?; or are mesic, epiphytic til- given lineage in both directions, would be re- landsioids derived from xeric precursors-Pit- gions where pluvial and arid climates have al- tendrigh's (1948) interpretation? Benzing also ternated. During the Pleistocene, pulsating, cli- considered a third interpretation, proposed by matic changes occurred at least in some parts Medina (1974) who examined carbon path- of South America (Haffer, 1969; Sarmiento, ways. Medina proposed that both xeric and 1975; Simpson, 1975; Solbrig, 1976; Gilmar- mesic tillandsioids arose from precursors tin, 1983). adapted to conditions of high light intensity With these ideas in mind, and using phy- and humidity. logenetic reconstruction methods, we exam- There is little support for the often held no- ined the possible direction(s) of evolution tion that xeric adaptations in general, are more among members of a closely related group of frequently acquired from mesic progenitors tillandsioid species. Tillandsia is a large bro- than the reverse. Some reasons for the notion meliad genus of mixed habit with its center of are the many examples in the world's deserts distribution in South America. The study group members are all epiphytic or saxicolous, in either case, nutritionally independent from the ' Received for publication 6 May 1985; revision ac- cepted 4 October 1985. substrate (Pittendrigh, 1948) and include me- Research supported by NSF Grant BSR 84407573 to sic, semi-mesic and xeric species. the authors. The following individuals provided extremely Species of Phytarrhiza with thin, flexible leaf- helpful critical reviews: David Benzing, Phil Cantino, Vicki blades 2.0 cm or more in width are considered Funk, Loren Rieseberg, Karen Simmons, Douglas Soltis, mesic termed and John Utley. Robin Lesher provided technical assis- as (Fig. la). Schimper (1908) tance and plant illustrations were rendered by Sheila Gil- mesic forms with leaf-rosettes capable of con- martin. taining water as tank epiphytes. Tank bro- 387 388 AMERICAN JOURNAL OF BOTANY [Vol. 73 N .=-"~~~~-~~---., .8 Fi. )Tyicliladsoifescaitb,em-m - . c C K41W? 811'a Fig. 1. a) Typical tillandsioid of mesic habit; b) semi-mesic habit; c) xeric habit. meliads retain a reservoirof water trappedby seek the answer in taxonomic revisions, and the leaf-rosetteand usually occupy moist areas by constructing cladograms and examining with mean annual precipitationof 200 to 400 patterns of morphological character-state cm, and in areaswhere no months receive less changes. than about 4%of the annualprecipitation (Gil- Phytarrhizainitially appearedto be mono- martin, 1973, 1983). Semi-mesic species have phyletic,unlike other Tillandsiasubgenera, e.g., a poorlydeveloped tank. Leaf-bladesare thick- Allardtia and Tillandsia, that could not be er and usually less than 2.0 cm wide (Fig. lb). shown to be natural groups (Gardner, 1982). They may flourishwhere annual precipitation Tillandsia Subg. Phytarrhizaspecies all share exceeds about 100 cm. Xeric species (Fig. lc) the uniquely derived petal-character,blades have no tank; leaf-bladesare very narrowand broadand conspicuous(Gilmartin, 1983), and succulent. Xeric tillandsioids can be expected is the only bromeliad group with conspicuous to occur in areas with a dry season and about petal-lamina. The three subgenera Diaphor- 30 to 100 cm annual precipitation (Rumley, anthema, Pseudo-Catopsis, and Phytarrhiza 1965; Gilmartin, 1972, 1973, 1983). all have very short styles that are includedwith We ask the question:within this group,which the stamens within the corolla. Togetherthese direction(s)of evolutionarychange, if any, oc- three subgeneraconstitute a putatively mono- curred most frequently:xerism toward mesic phyletic group. adaptations, or mesic forms toward xero- The relationshipof Phytarrhizato other til- phytes? In this first of a series of papers we landsioids has been a difficult question given March, 1986] GILMARTIN AND BROWN-TILLANDSIA. XEROPHYTES AND MESOPHYTES 389 previously available data and traditional an- forming the groups: leaf-blade width and de- alytical tools. This has not impeded specula- gree of succulence, and presence and devel- tion. The tools of modem phylogeneticrecon- opment of a tank. This was by design to avoid struction are brought to bear here on the circularity,so that resultingcladograms would question of relations of Phytarrhiza to other be based on other data than the very characters tillandsioids with focus on two of the most for which we hoped to discern polarity, i.e., likelycontenders for sistertaxon status.A sister direction of evolution. (The groups did not taxon is that evolutionaryunit sharingwith the changewhen the analysesincluded these char- groupunder study the same most recent com- acters.) mon ancestor. Its identification is one of the most effectivemeans to determinedirection of MATERIALSAND METHODS-Datawere as- evolution of characters(Hennig, 1966; Wiley, sembled from the Monograph by Smith and 1981), i.e., to establish which states are an- Downs (1977), and methods of phylogenetic central, which are derived. reconstructionwere applied under the princi- Strongtendencies toward parallelevolution ple of maximum parsimony (Wiley, 1981). are evident within every major group of or- Maximum parsimony has the goal of recon- ganisms. Among traits showing parallel evo- structing phylogeny with the fewest possible lution,those involvingless complexityare more character-statechanges for each character.The likely to exhibit reversals,i.e., change in more directions of change (character-statepolari- thana singledirection, than arethose involving ties), wereestablished using the two most likely greatercomplexity (Futuyma, 1979) and while alternative sister taxa, Subg. Pseudo-Catopsis both parallelsand reversals may occur, often and Subg.Diaphoranthema. This approachhas we expect more of the formerand fewer of the been described as the outgroup substitution latter. Stebbins' (1974) concepts of paths of method by Donoghue and Cantino (1984). least resistance may help to explain why par- These authors suggested using multiple out- allel evolutionary change occurs as frequently groupsalone and in combination to identify a as it does among related taxa. consensustree. Our objective is to identify the Parallelevolution is very common in flow- most likely hypothetical sister taxon, because ering plants (Cronquist, 1968; Funk, 1981), our central concern is the direction(s) of evo- and bromeliads are no exception (Benzing, lution relative to xerophytesand mesophytes. 1980; Gardner, 1982). For example phyloge- The study group is analyzed with the two al- netically isolated bromeliad taxa have several ternative sister taxa that prior research sug- times independentlyacquired nectar scales on gested. the ventral petal surface (Smith and Downs, Deployment of Diaphoranthemaas the sis- 1974, 1977, 1979). Parallel charactersshould ter taxon to Phytarrhizais implicit in Smith's not be removed however, before constructing remarks (1934) regardingthe apparent close- treesbecause they may be useful at branchtips ness of these two taxa.