Timothy M. Evans

Phylogeny, adaptive radiation, and historical biogeography in Bromeliaceae: Insights from an eight-locus plastid phylogeny

PREMISE Bromeliaceae form a large, ecologically diverse family of angiosperms native to the New World. We use a bromeliad phylogeny based on eight plastid regions to analyze relationships within the family, test a new, eight-subfamily classification, infer the chronology of bromeliad evolution and invasion of different regions, and provide the basis for future analyses of trait evolution and rates of diversification. METHODS We employed maximum-parsimony, maximum-likelihood, and Bayesian approaches to analyze 9341 aligned bases for four outgroups and 90 bromeliad species representing 46 of 58 described genera. We calibrate the resulting phylogeny against time using penalized likelihood applied to a monocot-wide tree based on plastid ndhF sequences and use it to analyze patterns of geographic spread using parsimony, Bayesian inference, and the program S-DIVA. RESULTS Bromeliad subfamilies are related to each other as follows: (Brocchinioideae, (Lindmanioideae, (Tillandsioideae, (Hechtioideae, (Navioideae, (Pitcairnioideae, (Puyoideae, Bromelioideae))))))). Bromeliads arose in the Guayana Shield ca. 100 million years ago (Ma), spread centrifugally in the New World beginning ca. 16-13 Ma, and dispersed to West Africa ca. 9.3 Ma. Modern lineages began to diverge from each other roughly 19 Ma. CONCLUSIONS Nearly two-thirds of extant bromeliads belong to two large radiations: the core tillandsioids, originating in the Andes ca. 14.2 Ma, and the Brazilian Shield bromelioids, originating in the Serro do Mar and adjacent regions ca. 9.1 Ma.

ANCIENT VICARIANCE OR RECENT LONG-DISTANCE DISPERSAL? INFERENCES ABOUT PHYLOGENY AND SOUTH AMERICAN-AFRICAN DISJUNCTIONS IN RAPATEACEAE AND BROMELIACEAE BASED ON ndhF SEQUENCE DATA

Rapateaceae and Bromeliaceae each have a center of diversity in South America and a single species native to a sandstone area in west Africa that abutted the Guayana Shield in northern South America before the Atlantic rifted. They thus provide ideal material for examining the potential role of vicariance versus long‐distance dispersal in creating amphiatlantic disjunctions. Analyses based on ndhF sequence variation indicate that Rapateaceae and Bromeliaceae are each monophyletic and underwent crown radiation around 41 and 23 Ma, respectively. Both exhibit clocklike sequence evolution, with bromeliads evolving roughly one‐third more slowly than rapateads. Among rapateads, the divergence of west African Maschalocephalus dinklagei from its closest South American relatives implies that Maschalocephalus resulted via long‐distance dispersal 7 Ma, not ancient continental drift; only its sandstone habitat is vicariant. Rapateads arose first at low elevations in the Guayana Shield; the earliest divergent genera are widespread along riverine corridors there and, to a lesser extent, in Amazonia and the Brazilian Shield. Speciation at small spatial scales accelerated 15 Ma with the invasion of high‐elevation, insular habitats atop tepuis. Among bromeliads, Pitcairnia feliciana diverges little from its congeners and appears to be the product of long‐distance dispersal ca. 12 Ma. Brocchinia/Ayensua and then Lindmania are sister to all other bromeliads, indicating that the Guayana Shield was also the cradle of the bromeliads. Three lineages form an unresolved trichotomy representing all other bromeliads: (1) Till andsioideae, (2) Hechtia, and (3) a large clade including remaining genera of Pitcairnioideae and all Bromelioideae. The last includes a clade of pitcairnioid genera endemic to the Guayana and Brazilian Shields; a xeric group (Abromeitiella/Deuterocohnia/Dyckia/Encholirium/Fosterella) from southern South America and the southern Andes, sister to Pitcairnia; and Andean Puya, sister to Bromelioideae, with many of the latter native to the Brazilian Shield. Both Rapateaceae and Bromeliaceae appear to have arisen at low elevations in the Guayana Shield, experienced accelerated speciation after invading dissected mountainous terrain, and undergone long‐distance dispersal to west Africa recently. Bromeliad acquisition of key adaptations to drought (e.g., CAM photosynthesis, tank habit, tillandsioid leaf trichomes) 17 Ma appears to have coincided with and help cause the centripetal invasion of drier, more seasonal regions beyond the Guayana Shield, resulting in a wider familial range and dominance of the epiphytic adaptive zone. Geology, past and present climate, and proximity to South America help account for both families occurring in nearly the same area of Africa. We present a new classification for Rapateaceae, including a new tribe Stegolepideae, a new subfamily Monotremoideae, and revisions to tribe Saxofridericieae and subfamily Rapateoideae.

Monophyly and Phylogenetic Relationships in Lymania (Bromeliaceae: Bromelioideae) Based on Morphology and Chloroplast DNA Sequences

Abstract A cladistic analysis of Lymania was conducted using morphology and sequences from three chloroplast DNA regions: the matK coding region and the psbA-trnH and trnL-trnF intergenic spacers. The monophyly of the genus and the phylogenetic relationships among related genera were examined. Of the nine Lymania species, eight are endemic to southern Bahia, Brazil. Lymania is the first genus in Bromeliaceae subfamily Bromelioideae to be subjected to a combined morphological and molecular analysis. The genera of Bromelioideae have been particularly difficult to classify and there has been disagreement about their interrelationships and monophyly. Morphological data show better resolution than molecular data alone. The partition homogeneity test supported a combined analysis of the two data sets, yielding a single most parsimonious tree. In the combined analysis, monophyly of Lymania is moderately supported, and the genus is closely related to species of Aechmea subg. Lamprococcus and subg. subg. Ortigiesia. The morphological distinctiveness coupled with low molecular divergence indicates relatively recent and rapid speciation within Lymania. The combined analysis of morphological and molecular data as done in this study provides a framework for future research on other Bromelioideae genera that could foster better taxonomic rearrangements.

Phylogenetic Relationships in the Commelinaceae: I. A Cladistic Analysis of Morphological Data

Abstract The plant family Commelinaceae displays a wide range of variation in vegetative, floral, and inflorescence morphology. This high degree of variation, particularly among characters operating under strong and similar selective pressures (i.e., flowers), has made the assessment of homology among morphological characters difficult, and has resulted in several discordant classification schemes for the family. Phylogenetic relationships among 40 of the 41 genera in the family were evaluated using cladistic analyses of morphological data. The resulting phylogeny shows some similarity to the most recent classification, but with some notable differences. Cartonema (subfamily Cartonematoideae) was placed basal to the rest of the family. Triceratella (subfamily Cartonematoideae), however, was placed among genera within tribe Tradescantieae of subfamily Commelinoideae. Likewise, the circumscriptions of tribes Commelineae and Tradescantieae were in disagreement with the most recent classification. The discordance between the phylogeny and the most recent classification is attributed to a high degree of convergence in various morphological characters, particularly those relating to the androecium and the inflorescence. Anatomical characters (i.e., stomatal structure), on the other hand, show promise for resolving phylogenetic relationships within the Commelinaceae, based upon their agreement with the most recent classification. Communicating Editor: Richard Jensen

Morphological and Molecular Evidence of Polyphyly in Rhodomyrtus (Myrtaceae: Myrteae)

Abstract The monophyly of the genus Rhodomyrtus (Myrtaceae) was tested using data from morphology and the nuclear ribosomal ITS regions (ITS-1, ITS-2) and 5.8S gene. Representative species from baccate genera hypothesized to be closely related to Rhodomyrtus were included, such as Archirhodomyrtus, Octamyrtus, Knnakomyrtus, and some genera believed to be more distantly related, including Rhodamnia, Decaspermum, Pilidiostigma, and Myrtastrum. Up to four capsular-fruited outgroup species were used to root the trees (Heteropyxis natalensis, Carpolepis tardiflora, Lophostemon confertus, and Metrosideros rotundifolia). Morphological data using neighbor joining scattered species of Rhodomyrtus across several branches but generally recovered genera other than Rhodomyrtus. Using parsimony, the morphological data analysis also rejected the monophyly of Rhodomyrtus and resulted in consensus trees with relatively low resolution and bootstrap support. Based on traditionally recognized generic boundaries, results from DNA sequence data (parsimony, Bayesian analysis) rejected the hypothesized monophyly of Rhodomyrtus and typically dispersed species of Rhodomyrtus irregularly into two relatively large branches designated as Clades A and B. Species other than Rhodomyrtus contained in either Clade A or B from the molecular results were some, but not all, members of Archirhodomyrtus, Octamyrtus, and Knnakomyrtus. Partition tests indicated that phylogenies based on morphological characters differed significantly from those based on molecular data so a combined analysis was not conducted. DNA sequence variation ranged from no variation among sequences within a species up to 61 base pair differences plus four 1 or 2 bp gaps between Rhodomyrtus misimana and R. mcmtana. Although results from morphological and molecular analyses reject the hypothesis that Rhodomyrtus is monophyletic, additional data are needed before Rhodomyrtus can be split confidently into demonstrably monophyletic genera.

Phylogenetic Relationships in Bromeliaceae Subfamily Bromelioideae based on Chloroplast DNA Sequence Data

Abstract Of the eight subfamilies currently recognized in Bromeliaceae, Bromelioideae is perhaps the most poorly understood. Generic circumscriptions are unclear, and an exceptionally diverse morphology coupled with an unusually low rate of sequence divergence within Bromeliaceae has made it difficult to resolve phylogenetic relationships within the subfamily. Although recent molecular studies have begun elucidating relationships among species in Bromeliaceae, most have not sampled deeply and/or broadly across Bromelioideae. The purpose of this study was to conduct a phylogenetic analysis within subfamily Bromelioideae using three chloroplast DNA regions (matK, psbA-trnH, and trnL-trnF), with the inclusion of multiple species from a broad sampling of bromelioid genera. Ochagavia, Deinacanthon, Fascicularia, Bromelia and Fernseea diverged relatively early in the history of the subfamily, with the remaining taxa being placed in a large and poorly resolved eubromelioid clade. Bromelia and Cryptanthus were found to be monophyletic, while 13 other genera were polyphyletic. Aechmea, the most morphologically diverse genus within the subfamily, was highly polyphyletic, with species distributed among 12 different lineages, with little support for subgeneric circumscriptions.

Plicate Staminal Filaments in Tillandsia Subgenus Anoplophytum (Bromeliaceae)

Plication of staminal filaments is an important diagnostic character for Tillandsia subgenus Anoplophytum (ca. 45 species). The monophyletic integrity of subgenus Anoplophytum has recently been questioned, and we conducted an anatomical investigation of plicate staminal filaments to better characterize this putative synapomorphy. Developmental studies show that the filament plications, or folds, become visible during or soon after anthesis. Serial sections of preplication filaments and filaments in sequential stages of plication were prepared and observed with light microscopy. A uniform sequence of parenchyma cell collapse begins three to four cell layers out from the vascular bundle and proceeds centrifugally to the epidermis. Eventually the epidermal cells collapse, leaving only the vascular bundle and a few surrounding parenchyma cells intact. Above and below the zone of plication, all parenchyma and epidermal cells in the filament remain intact. Species traditionally placed in subgenera Tillandsia and Allardtia have been found with plicate staminal filaments that are anatomically and developmentally identical to those studied from subgenus Anoplophytum. Alone, staminal filament plication does not appear to be a good diagnostic character for subgenus Anoplophytum, and doubts concerning the monophylesis of this subgenus are reinforced. The functional significance of stamen filament plication remains unknown.