Kenneth J. Wurdack

Angiosperm phylogeny: 17 genes, 640 taxa

PREMISE OF THE STUDY Recent analyses employing up to five genes have provided numerous insights into angiosperm phylogeny, but many relationships have remained unresolved or poorly supported. In the hope of improving our understanding of angiosperm phylogeny, we expanded sampling of taxa and genes beyond previous analyses. METHODS We conducted two primary analyses based on 640 species representing 330 families. The first included 25260 aligned base pairs (bp) from 17 genes (representing all three plant genomes, i.e., nucleus, plastid, and mitochondrion). The second included 19846 aligned bp from 13 genes (representing only the nucleus and plastid). KEY RESULTS Many important questions of deep-level relationships in the nonmonocot angiosperms have now been resolved with strong support. Amborellaceae, Nymphaeales, and Austrobaileyales are successive sisters to the remaining angiosperms (Mesangiospermae), which are resolved into Chloranthales + Magnoliidae as sister to Monocotyledoneae + [Ceratophyllaceae + Eudicotyledoneae]. Eudicotyledoneae contains a basal grade subtending Gunneridae. Within Gunneridae, Gunnerales are sister to the remainder (Pentapetalae), which comprises (1) Superrosidae, consisting of Rosidae (including Vitaceae) and Saxifragales; and (2) Superasteridae, comprising Berberidopsidales, Santalales, Caryophyllales, Asteridae, and, based on this study, Dilleniaceae (although other recent analyses disagree with this placement). Within the major subclades of Pentapetalae, most deep-level relationships are resolved with strong support. CONCLUSIONS Our analyses confirm that with large amounts of sequence data, most deep-level relationships within the angiosperms can be resolved. We anticipate that this well-resolved angiosperm tree will be of broad utility for many areas of biology, including physiology, ecology, paleobiology, and genomics.

Phylogeny of the eudicots : a nearly complete familial analysis based on rbcL gene sequences

A phylogenetic analysis of 589 plastid rbcL gene sequences representing nearly all eudicot families (a total of 308 families; seven photosynthetic and four parasitic families are missing) was performed, and bootstrap re-sampling was used to assess support for clades. Based on these data, the ordinal classification of eudicots is revised following the previous classification of angiosperms by the Angiosperm Phylogeny Group (APG). Putative additional orders are discussed (e.g. Dilleniales, Escalloniales, Vitales), and several additional families are assigned to orders for future updates of the APG classification. The use of rbcL alone in such a large matrix was found to be practical in discovering and providing bootstrap support for most orders. Combination of these data with other matrices for the rest of the angiosperms should provide the framework for a complete phylogeny to be used in macro-evolutionary studies.

Explosive radiation of Malpighiales supports a mid-cretaceous origin of modern tropical rain forests.

Fossil data have been interpreted as indicating that Late Cretaceous tropical forests were open and dry adapted and that modern closed‐canopy rain forest did not originate until after the Cretaceous‐Tertiary (K/T) boundary. However, some mid‐Cretaceous leaf floras have been interpreted as rain forest. Molecular divergence‐time estimates within the clade Malpighiales, which constitute a large percentage of species in the shaded, shrub, and small tree layer in tropical rain forests worldwide, provide new tests of these hypotheses. We estimate that all 28 major lineages (i.e., traditionally recognized families) within this clade originated in tropical rain forest well before the Tertiary, mostly during the Albian and Cenomanian (112–94 Ma). Their rapid rise in the mid‐Cretaceous may have resulted from the origin of adaptations to survive and reproduce under a closed forest canopy. This pattern may also be paralleled by other similarly diverse lineages and supports fossil indications that closed‐canopy tropical rain forests existed well before the K/T boundary. This case illustrates that dated phylogenies can provide an important new source of evidence bearing on the timing of major environmental changes, which may be especially useful when fossil evidence is limited or controversial.

Malpighiales phylogenetics: gaining ground on one of the most recalcitrant clades in the angiosperm tree of life.

The eudicot order Malpighiales contains ∼16000 species and is the most poorly resolved large rosid clade. To clarify phylogenetic relationships in the order, we used maximum likelihood, Bayesian, and parsimony analyses of DNA sequence data from 13 gene regions, totaling 15604 bp, and representing all three genomic compartments (i.e., plastid: atpB, matK, ndhF, and rbcL; mitochondrial: ccmB, cob, matR, nad1B-C, nad6, and rps3; and nuclear: 18S rDNA, PHYC, and newly developed low-copy EMB2765). Our sampling of 190 taxa includes representatives from all families of Malpighiales. These data provide greatly increased support for the recent additions of Aneulophus, Bhesa, Centroplacus, Ploiarium, and Rafflesiaceae to Malpighiales; sister relations of Phyllanthaceae + Picrodendraceae, monophyly of Hypericaceae, and polyphyly of Clusiaceae. Oxalidales + Huaceae, followed by Celastrales are successive sisters to Malpighiales. Parasitic Rafflesiaceae, which produce the worlds largest flowers, are confirmed as embedded within a paraphyletic Euphorbiaceae. Novel findings show a well-supported placement of Ctenolophonaceae with Erythroxylaceae + Rhizophoraceae, sister-group relationships of Bhesa + Centroplacus, and the exclusion of Medusandra from Malpighiales. New taxonomic circumscriptions include the addition of Bhesa to Centroplacaceae, Medusandra to Peridiscaceae (Saxifragales), Calophyllaceae applied to Clusiaceae subfamily Kielmeyeroideae, Peraceae applied to Euphorbiaceae subfamily Peroideae, and Huaceae included in Oxalidales.

When in doubt, put it in Flacourtiaceae: a molecular phylogenetic analysis based on plastid rbcL DNA sequences

Summary. Circumscription of Flacourtiaceae was investigated with a phylogenetic analysis of plastid rbcL DNA sequences, and the family was found to be composed of two clades that are more closely related to other families in Malpighiales than to each other. In one of these, that containing the type genus Flacourtia, Salicaceae are embedded, whereas the other clade includes the members of the peculiar and poorly known South African Achariaceae. The latter family name is conserved against all listed synonyms. Thus we propose the recognition of two families: i) Salicaceae sensu lato, including tribes Banareae, Bembicieae, Scolopieae, Samydeae (syn. Casearieae), Homalieae, Flacourtieae, Prockieae and Saliceae, as well as Abatieae (by some authors of Passifloraceae) and Scyphostegieae (Scyphostegia of the monogeneric Scyphostegiaceae); and ii) Achariaceae sensu lato, including tribes Pangieae, Lindackerieae, Erythrospermeae and Acharieae (Acharia, Ceratiosicyos and Guthriea of Achariaceae). Several genera considered by many previous authors to be members of Flacourtiaceae are excluded from Malpighiales: Berberidopsis and Aphloia fall near the base of the higher eudicots. Several tribes require different names from those used in previous systems, and we include an appendix indicating a tentative revised tribal taxonomy for both Salicaceae and Achariaceae sensu lato.

Molecular phylogenetic analysis of uniovulate Euphorbiaceae (Euphorbiaceae sensu stricto) using plastid RBCL and TRNL-F DNA sequences

Parsimony and Bayesian analyses of plastid rbcL and trnL-F DNA sequence data of the pantropical family Euphorbiaceae sensu stricto (s.s.) are presented. Sampling includes representatives of all three subfamilies (Acalyphoideae, Crotonoideae, and Euphorbioideae), 35 of 37 tribes and 179 of the 247 genera of uniovulate Euphorbiaceae sensu lato (s.l.). Euphorbiaceae s.s. were recovered as a monophyletic group with no new adjustments in circumscription. Two clades containing taxa previously placed in Acalyphoideae are found to be successive sisters to all other Euphorbiaceae s.s. and are proposed here at subfamilial rank as Peroideae and Cheilosoideae. The remainder of the family fall into seven major lineages including Erismantheae and Acalyphoideae s.s. (parts of Acalyphoideae), Adenoclineae s.l., Gelonieae, articulated crotonoids and inaperturate crotonoids (parts of Crotonoideae), and Euphorbioideae. Potential synapomorphies and biogeographical trends are suggested for these clades. Acalyphoideae s.s., inaperturate crotonoids, and Euphorbioideae tribe Hippomaneae each have two major subclades that represent novel groupings without apparent morphological synapomorphies. Two subfamilies, 14 tribes, and 10 genera were found to be para- or polyphyletic. Noteworthy among these, Omphaleae are embedded in Adenoclineae, Hureae + Pachystromateae in Hippomaneae, Ditta in Tetrorchidium, and Sapium s.s. in Stillingia.

Phylogenomics and a posteriori data partitioning resolve the Cretaceous angiosperm radiation Malpighiales

The angiosperm order Malpighiales includes ∼16,000 species and constitutes up to 40% of the understory tree diversity in tropical rain forests. Despite remarkable progress in angiosperm systematics during the last 20 y, relationships within Malpighiales remain poorly resolved, possibly owing to its rapid rise during the mid-Cretaceous. Using phylogenomic approaches, including analyses of 82 plastid genes from 58 species, we identified 12 additional clades in Malpighiales and substantially increased resolution along the backbone. This greatly improved phylogeny revealed a dynamic history of shifts in net diversification rates across Malpighiales, with bursts of diversification noted in the Barbados cherries (Malpighiaceae), cocas (Erythroxylaceae), and passion flowers (Passifloraceae). We found that commonly used a priori approaches for partitioning concatenated data in maximum likelihood analyses, by gene or by codon position, performed poorly relative to the use of partitions identified a posteriori using a Bayesian mixture model. We also found better branch support in trees inferred from a taxon-rich, data-sparse matrix, which deeply sampled only the phylogenetically critical placeholders, than in trees inferred from a taxon-sparse matrix with little missing data. Although this matrix has more missing data, our a posteriori partitioning strategy reduced the possibility of producing multiple distinct but equally optimal topologies and increased phylogenetic decisiveness, compared with the strategy of partitioning by gene. These approaches are likely to help improve phylogenetic resolution in other poorly resolved major clades of angiosperms and to be more broadly useful in studies across the Tree of Life.

Molecular phylogenetics of the giant genus Croton and tribe Crotoneae (Euphorbiaceae sensu stricto) using ITS and TRNL-TRNF DNA sequence data

Parsimony, likelihood, and Bayesian analyses of nuclear ITS and plastid trnL-F DNA sequence data are presented for the giant genus Croton (Euphorbiaceae s.s.) and related taxa. Sampling comprises 88 taxa, including 78 of the estimated 1223 species and 29 of the 40 sections previously recognized of Croton. It also includes the satellite genus Moacroton and genera formerly placed in tribe Crotoneae. Croton and all sampled segregate genera form a monophyletic group sister to Brasiliocroton, with the exception of Croton sect. Astraea, which is reinstated to the genus Astraea. A small clade including Moacroton, Croton alabamensis, and C. olivaceus is sister to all other Croton species sampled. The remaining Croton species fall into three major clades. One of these is entirely New World, corresponding to sections Cyclostigma, Cascarilla, and Velamea sensu Webster. The second is entirely Old World and is sister to a third, also entirely New World clade, which is composed of at least 13 of Websters sections of Croton. This study establishes a phylogenetic framework for future studies in the hyper-diverse genus Croton, indicates a New World origin for the genus, and will soon be used to evaluate wood anatomical, cytological, and morphological data in the Crotoneae tribe.

Molecular Phylogenetics of Phyllanthaceae: Evidence from Plastid MatK and Nuclear PHYC Sequences

Plastid matK and a fragment of the low-copy nuclear gene PHYC were sequenced for 30 genera of Phyllanthaceae to evaluate tribal and generic delimitation. Resolution and bootstrap percentages obtained with matK are higher than that of PHYC, but both regions show nearly identical phylogenetic patterns. Phylogenetic relationships inferred from the independent and combined data are congruent and differ from previous, morphology-based classifications but are highly concordant with those of the plastid gene rbcL previously published. Phyllanthaceae is monophyletic and gives rise to two well-resolved clades (T and F) that could be recognized as subfamilies. DNA sequence data for Keayodendron and Zimmermanniopsis are presented for the first time. Keayodendron is misplaced in tribe Phyllantheae and belongs to the Bridelia alliance. Zimmermanniopsis is sister to Zimmermannia. Phyllanthus and Cleistanthus are paraphyletic. Savia and Phyllanthus subgenus Kirganelia are not monophyletic.

Floral Gigantism in Rafflesiaceae

Species of Rafflesiaceae possess the worlds largest flowers (up to 1 meter in diameter), yet their precise evolutionary relationships have been elusive, hindering our understanding of the evolution of their extraordinary reproductive morphology. We present results of phylogenetic analyses of mitochondrial, nuclear, and plastid data showing that Rafflesiaceae are derived from within Euphorbiaceae, the spurge family. Most euphorbs produce minute flowers, suggesting that the enormous flowers of Rafflesiaceae evolved from ancestors with tiny flowers. Given the inferred phylogeny, we estimate that there was a circa 79-fold increase in flower diameter on the stem lineage of Rafflesiaceae, making this one of the most dramatic cases of size evolution reported for eukaryotes.