Person:

Davis, Charles

The evolution of floral zygomorphy is an important innovation in flowering plants and is thought to arise principally from specialization on various insect pollinators. Floral morphology of neotropical Malpighiaceae is distinctive and highly conserved, especially with regard to symmetry, and is thought to be caused by selection by its oil-bee pollinators. We sought to characterize the genetic basis of floral zygomorphy in Malpighiaceae by investigating CYCLOIDEA2-like (CYC2-like) genes, which are required for establishing symmetry in diverse core eudicots. We identified two copies of CYC2-like genes in Malpighiaceae, which resulted from a gene duplication in the common ancestor of the family. A likely role for these loci in the development of floral zygomorphy in Malpighiaceae is demonstrated by the conserved pattern of dorsal gene expression in two distantly related neotropical species, Byrsonima crassifolia and Janusia guaranitica. Further evidence for this function is observed in a Malpighiaceae species that has moved to the paleotropics and experienced coincident shifts in pollinators, floral symmetry, and CYC2-like gene expression. The dorsal expression pat-tern observed in Malpighiaceae contrasts dramatically with their actinomorphic-flowered relatives, Centroplacaceae (Bhesa paniculata) and Elatinaceae (Bergia texana). In particular, B. texana exhibits a previously undescribed pattern of uniform CYC2 expression, suggesting that CYC2 expression among the actinomorphic ancestors of zygomorphic lineages may be much more complex than previously thought. We consider three evolutionary models that may have given rise to this patterning, including the hypothesis that floral zygomorphy in Malpighiaceae arose earlier than standard morphology-based character reconstructions suggest.

Premise of the study: The Malpighiaceae include ∼1300 tropical flowering plant species in which generic definitions and intergeneric relationships have long been problematic. The goals of our study were to resolve relationships among the 11 generic segregates from the New World genus Mascagnia, test the monophyly of the largest remaining Malpighiaceae genera, and clarify the placement of Old World Malpighiaceae.

Methods: We combined DNA sequence data for four genes (plastid ndhF, matK, and rbcL and nuclear PHYC) from 338 ingroup accessions that represented all 77 currently recognized genera with morphological data from 144 ingroup species to produce a complete generic phylogeny of the family.

Key results and conclusions: The genera are distributed among 14 mostly well-supported clades. The interrelationships of these major subclades have strong support, except for the clade comprising the wing-fruited genera (i.e., the malpighioid+Amorimia, Ectopopterys, hiraeoid, stigmaphylloid, and tetrapteroid clades). These results resolve numerous systematic problems, while others have emerged and constitute opportunities for future study. Malpighiaceae migrated from the New to Old World nine times, with two of those migrants being very recent arrivals from the New World. The seven other Old World clades dispersed much earlier, likely during the Tertiary. Comparison of floral morphology in Old World Malpighiaceae with their closest New World relatives suggests that morphological stasis in the New World likely results from selection by neotropical oil-bee pollinators and that the morphological diversity found in Old World flowers has evolved following their release from selection by those bees.

Malpighiaceae possess flowers with a unique bilateral symmetry (zygomorphy), which is a hypothesized adaptation associated with specialization on neotropical oil bee pollinators. Gene expression of two representatives of the CYC2 lineage of floral symmetry TCP genes, CYC2A and CYC2B, demarcate the adaxial (dorsal) region of the flower in the characteristic zygomorphic flowers of most Malpighiaceae. Several clades within the family, however, have independently lost their specialized oil bee pollinators and reverted to radial flowers (actinomorphy) like their ancestors. Here, we investigate CYC2 expression associated with four independent reversals to actinomorphy. We demonstrate that these reversals are always associated with alteration of the highly conserved CYC2 expression pattern observed in most New World (NW) Malpighiaceae. In NW Lasiocarpus and Old World (OW) Microsteria, the expression of CYC2-like genes has expanded to include the ventral region of the corolla. Thus, the pattern of gene expression in these species has become radialized, which is comparable to what has been reported in the radial flowered legume clade Cadia. In striking contrast, in NW Psychopterys and OW Sphedamnocarpus, CYC2-like expression is entirely absent or at barely detectable levels. This is more similar to the pattern of CYC2 expression observed in radial flowered Arabidopsis. These results collectively indicate that, regardless of geographic distribution, reversals to similar floral phenotypes in this large tropical angiosperm clade have evolved via different genetic changes from an otherwise highly conserved developmental program.

Phylogenetic analyses of molecular and morphological data have shown the genus Banisteriopsis to be polyphyletic and the genus Diplopterys to be nested within Banisteriopsis subg. Pleiopterys, which is not in the clade that contains the type of the name Banisteriopsis. Therefore, it is necessary to take up the name Diplopterys for the small genus formerly called that plus subg. Pleiopterys of Banisteriopsis. Adescription of the amplified genus Diplopterys is provided, two new species are described (D. bahianaand and D. carvalhoi), and the following new combinations in Diplopterysare proposed, with all combinations by W. R. Anderson and C. Cav. Davis: D. amplectens, D. cachimbensis, D. caduciflora, D. cristata,D. erianthera, D. heterostyla, D. hypericifolia, D. krukoffii, D. leiocarpa, D. longialata, D. lucida, D. lutea, D. nigrescens, D. nutans, D. patula, D. peruviana, D. platyptera, D. populifolia, D. pubipetala, D. rondoniensis, D. schunkei, D. sepium, D. valvata, D. virgultosa, and D. woytkowskii. Illustrations are provided for D. bahiana, D. cabrerana, D. carvalhoi, D. pauciflora, D. pubipetala, and D. valvata.

Phylogenetic data from plastid (ndhF and rbcL) and nuclear (PHYC) genes indicate that, within the order Malpighiales, Elatinaceae are strongly supported as sister to Malpighiaceae. There are several putative morphological synapomorphies for this clade; most notably, they both have a base chromosome number of X = 6 (or some multiple of three or six), opposite or whorled leaves with stipules, unicellular hairs (also uniseriate in some Elatinaceae), multicellular glands on the leaves, and resin (Elatinacae) or latex (Malpighiaceae). Further study is needed to determine if these features are synapomorphic within the order. Malpighiaceae have previously been inferred as sister to Peridiscaceae based on rbcL sequence data, but the rbcL sequence of Whittonia is a chimera of two sequences, neither of which appears to be Whittonia. Our data from plastid (atpB, rbcL) and nuclear (18S rDNA) genes instead place Peridiscaeace as a member of the Saxifragales.

The Malpighiaceae are a family of similar to ~1250 species of predominantly New World tropical flowering plants. Infrafamilial classification has long been based on fruit characters. Phylogenetic analyses of chloroplast DNA nucleotide sequences were analyzed to help resolve the phylogeny of Malpighiaceae. A total of 79 species. representing 58 of the 65 currently recognized genera. were studied. The 3' region of the gene ndhF was sequenced for 77 species and the noncoding intergenic spacer region trnL-F was sequenced for 65 species' both sequences were obtained for the outgroup, Humiria (Humiriaceae), Phylogenetic relationships inferred from these data,ets are largely congruent with one another and with results from combined analyses. The family is divided into two major clades, recognized here as the subfamilies Byrsonimoideae (New World only) and Malpighioideae (New World and Old World). Niedenzu's tribes are all polyphyletic, suggesting extensive convergence on similar fruit types; only de Jussieu's tribe Gaudichaudieae and Anderson's tribes Acmanthereae and Galphimieae are monophyletic. Fleshy fruits evolved three times in the family and bristly fruits at least three times. Among the wing-fruited vines, which constitute more than half the diversity in the family, genera with dorsal-winged samaras are fairly well resolved, while the resolution of taxa with lateral-winged samaras is poor. The trees suggest a shift from radially symmetrical pollen arrangement to globally symmetrical pollen at the base of one of the clades within the Malpighioideae. The Old World taxa fall into at least six and as many as nine clades.

Madagasikaria andersonii is described here as a new genus and species of Malpighiaceae from Madagascar. The phylogenetic placement of Madagasikaria was estimated by using combined data from ndhF and trnL-F chloroplast sequences and phytochrome (PHYC) and ITS nuclear sequences. It forms a strongly supported clade with the Malagasy endemic genera Rhynchophora and Microsteira. Despite nearly identical floral morphology among species in this elude (here called the madagasikarioid clade), these genera are easily distinguishable on the basis of their fruits, The schizocarpic fruits of Madagasikaria have distinctive mericarps. Each mericarp has a lateral wing, which completely encircles the nut, and a peculiar dorsal wing, which folds over on itself. The morphology of this fruit suggests that the homology of the unusual wing in Rhyncnophora is lateral in nature and represents a reduced wing similar to the lateral wing in Madagasikaria. Taxa in the madagasikarioid clade all appear to be morphologically androdioecious and functionally dioecious, producing both staminate and "bisexual" (i.e., functionally carpeliate) individuals. This condition appears to be exceedingly rare in flowering plants and has important implications for floral evolution within Malpighiaccae. Neotropical Malpighiaceae are pollinated by specialized oil-collecting anthophorine bees of the tribe Centridini and exhibit highly conserved floral morphology despite tremendous diversity in fruit morphology and habit. These oil-collecting bees are absent from the paleotropics, where most members of the Malpighiaceae lack both the oil glands and the typical floral orientation crucial to pollination by neotropical oil-collecting bees. The madagasikarioids represent one shift from the neotropical pollination syndrome among Old World Malpighiaceae.