Bryan T. Drew

Synthesis of phylogeny and taxonomy into a comprehensive tree of life

Significance Scientists have used gene sequences and morphological data to construct tens of thousands of evolutionary trees that describe the evolutionary history of animals, plants, and microbes. This study is the first, to our knowledge, to apply an efficient and automated process for assembling published trees into a complete tree of life. This tree and the underlying data are available to browse and download from the Internet, facilitating subsequent analyses that require evolutionary trees. The tree can be easily updated with newly published data. Our analysis of coverage not only reveals gaps in sampling and naming biodiversity but also further demonstrates that most published phylogenies are not available in digital formats that can be summarized into a tree of life. Reconstructing the phylogenetic relationships that unite all lineages (the tree of life) is a grand challenge. The paucity of homologous character data across disparately related lineages currently renders direct phylogenetic inference untenable. To reconstruct a comprehensive tree of life, we therefore synthesized published phylogenies, together with taxonomic classifications for taxa never incorporated into a phylogeny. We present a draft tree containing 2.3 million tips—the Open Tree of Life. Realization of this tree required the assembly of two additional community resources: (i) a comprehensive global reference taxonomy and (ii) a database of published phylogenetic trees mapped to this taxonomy. Our open source framework facilitates community comment and contribution, enabling the tree to be continuously updated when new phylogenetic and taxonomic data become digitally available. Although data coverage and phylogenetic conflict across the Open Tree of Life illuminate gaps in both the underlying data available for phylogenetic reconstruction and the publication of trees as digital objects, the tree provides a compelling starting point for community contribution. This comprehensive tree will fuel fundamental research on the nature of biological diversity, ultimately providing up-to-date phylogenies for downstream applications in comparative biology, ecology, conservation biology, climate change, agriculture, and genomics.

Phylogenetics, biogeography, and staminal evolution in the tribe Mentheae (Lamiaceae)

PREMISE OF THE STUDY The mint family (Lamiaceae) is the sixth largest family of flowering plants, with the tribe Mentheae containing about a third of the species. We present a detailed perspective on the evolution of the tribe Mentheae based on a phylogenetic analysis of cpDNA and nrDNA that is the most comprehensive to date, a biogeographic set of analyses using a fossil-calibrated chronogram, and an examination of staminal evolution. METHODS Data from four cpDNA and two nrDNA markers representing all extant genera within the tribe Mentheae were analyzed using the programs BEAST, Lagrange, S-DIVA, and BayesTraits. BEAST was used to simultaneously estimate phylogeny and divergence times, Lagrange and S-DIVA were used for biogeographical reconstruction, and BayesTraits was used to infer staminal evolution within the tribe. KEY RESULTS Currently accepted subtribal delimitations are shown to be invalid and are updated. The Mentheae and all five of its subtribes have a Mediterranean origin and have dispersed to the New World multiple times. The vast majority of New World species of subtribe Menthinae are the product of a single dispersal event in the mid-late Miocene. At least four transitions from four stamens to two stamens have occurred within Mentheae, once in the subtribe Salviinae, once in the subtribe Lycopinae, and at least twice in the subtribe Menthinae. CONCLUSIONS Worldwide cooling trends probably played a large role in the diversification and present day distribution of the tribe Mentheae. Additional work is needed to ascertain relationships within some Mentheae genera, especially in the subtribe Menthinae.

Lost branches on the tree of life.

Failure to archive published data can impede reproducibility and inhibit downstream synthesis. Alarmingly, we estimate that ∼70% of existing DNA sequence alignments/phylogenetic trees, representing much of the underpinning of modern phylogenetic analysis, are no longer accessible. The evolutionary biology community needs to adopt policies ensuring that data are publicly archived upon publication.

Evolution of secondary heads in Nassauviinae (Asteraceae, Mutisieae)

The evolution of the inflorescence head in Asteraceae is important in the diversification of this largest angiosperm family. The aggregation of heads into higher-order capitulescences (secondary heads or syncephalia) is considered evolutionarily advanced. The genera Moscharia, Nassauvia, Polyachyrus, and Triptilion of the subtribe Nassauviinae (Mutisieae) have syncephalia with differing degrees of capitula condensation. ITS and plastid trnL-trnF regions were analyzed separately and together using maximum parsimony and maximum likelihood to examine the evolution of syncephalia in the Nassauviinae. The four genera displaying syncephalia do not form a clade minus taxa without syncephalia, indicating that secondary heads in Nassauviinae have either convergently evolved twice in the subtribe (or, very unlikely) once with multiple reversions. Strong support was obtained for a sister relationship between Leucheria (without syncephalium) and Polyachyrus, and both sister to Moscharia. Nassauvia and Triptilion form a distinct clade but are sister to other genera, Perezia and Panphalea, without syncephalium. Previous hypotheses postulated the evolution from simple to more complex secondary heads. We show that the ancestor of Moscharia, Polyachyrus, and Leucheria, in a more arid habitat, had a complex type of secondary head, and loss of complexity occurred in response to a shift from arid to mesic conditions.

Phylogeny, divergence times, and historical biogeography of the angiosperm family Saxifragaceae

Saxifragaceae (Saxifragales) contain approximately 640 species and 33 genera, about half of which are monotypic. Due to factors such as morphological stasis, convergent morphological evolution, and disjunct distributions, relationships within Saxifragaceae have historically been troublesome. The family occurs primarily in mountainous regions of the Northern Hemisphere, with the highest generic and species diversity in western North America, but disjunct taxa are known from southern South America. Here, we integrate broad gene (56 loci) and taxon (223 species) sampling strategies, both the most comprehensive to date within Saxifragaceae, with fossil calibrations and geographical distribution data to address relationships, divergence times, and historical biogeography among major lineages of Saxifragaceae. Two previously recognized main clades, the heucheroids (eight groups+Saniculiphyllum) and saxifragoids (Saxifraga s.s.), were re-affirmed by our phylogenetic analyses. Relationships among the eight heucheroid groups, as well as the phylogenetic position of Saniculiphyllum within the heucheroids, were resolved with mostly high support. Divergence time estimates indicate that Saxifragaceae began to diversify ca. 38.37 million years ago (Mya; 95% HPD=30.99-46.11Mya) in the Mid-Late Eocene, and that the two major lineages, the heucheroids and saxifragoids, began to diversify approximately 30.04Mya (95% HPD=23.87-37.15Mya) and 30.85 Mya (95% HPD=23.47-39.33Mya), respectively. We reconstructed ancestral geographic areas using statistical dispersal-vicariance (S-DIVA). These analyses indicate several radiations within Saxifragaceae: one in eastern Asia and multiple radiations in western North America. Our results also demonstrate that large amounts of sequence data coupled with broad taxon sampling can help resolve clade relationships that have thus far seemed intractable.

Does the Arcto-Tertiary Biogeographic Hypothesis Explain the Disjunct Distribution of Northern Hemisphere Herbaceous Plants? The Case of Meehania (Lamiaceae)

Despite considerable progress, many details regarding the evolution of the Arcto-Tertiary flora, including the timing, direction, and relative importance of migration routes in the evolution of woody and herbaceous taxa of the Northern Hemisphere, remain poorly understood. Meehania (Lamiaceae) comprises seven species and five subspecies of annual or perennial herbs, and is one of the few Lamiaceae genera known to have an exclusively disjunct distribution between eastern Asia and eastern North America. We analyzed the phylogeny and biogeographical history of Meehania to explore how the Arcto-Tertiary biogeographic hypothesis and two possible migration routes explain the disjunct distribution of Northern Hemisphere herbaceous plants. Parsimony and Bayesian inference were used for phylogenetic analyses based on five plastid sequences (rbcL, rps16, rpl32-trnH, psbA-trnH, and trnL-F) and two nuclear (ITS and ETS) gene regions. Divergence times and biogeographic inferences were performed using Bayesian methods as implemented in BEAST and S-DIVA, respectively. Analyses including 11 of the 12 known Meehania taxa revealed incongruence between the chloroplast and nuclear trees, particularly in the positions of Glechoma and Meehania cordata, possibly indicating allopolyploidy with chloroplast capture in the late Miocene. Based on nrDNA, Meehania is monophyletic, and the North American species M. cordata is sister to a clade containing the eastern Asian species. The divergence time between the North American M. cordata and the eastern Asian species occurred about 9.81 Mya according to the Bayesian relaxed clock methods applied to the combined nuclear data. Biogeographic analyses suggest a primary role of the Arcto-Tertiary flora in the study taxa distribution, with a northeast Asian origin of Meehania. Our results suggest an Arcto-Tertiary origin of Meehania, with its present distribution most probably being a result of vicariance and southward migrations of populations during climatic oscillations in the middle Miocene with subsequent migration into eastern North America via the Bering land bridge in the late Miocene.

Systematics, biogeography, and character evolution of Sparganium (Typhaceae): Diversification of a widespread, aquatic lineage

UNLABELLED PREMISE OF THE STUDY Sparganium (Typhaceae) is a genus of aquatic monocots containing ±14 species, with flowers aggregated in unisexual, spherical heads, and habit ranging from floating to emergent. Sparganium presents an opportunity to investigate diversification, character evolution, and biogeographical relationships in a widespread temperate genus of aquatic monocots. We present a fossil-calibrated, molecular phylogeny of Sparganium based on analysis of two chloroplast and two nuclear markers. Within this framework, we examine character evolution in both habit and stigma number and infer the ancestral area and biogeographic history of the genus. • METHODS Sequence data from two cpDNA and two nDNA markers were analyzed using maximum parsimony, maximum likelihood, and Bayesian inference. We used the program BEAST to simultaneously estimate phylogeny and divergence times, S-DIVA and Lagrange for biogeographical reconstruction, and BayesTraits to examine locule number and habit evolution. • KEY RESULTS Two major clades were recovered with strong support: one composed of S. erectum and S. eurycarpum; and the other containing all remaining Sparganium. We realigned the subgenera to conform to these clades. Divergence time analysis suggests a Miocene crown origin but Pliocene diversification. Importantly, the floating-leaved habit has arisen multiple times in the genus, from emergent ancestors-contrary to past hypotheses. • CONCLUSIONS Cooling trends during the Tertiary are correlated with the isolation of temperate Eurasian and North American taxa. Vicariance, long-distance dispersal, and habitat specialization are proposed as mechanisms for Sparganium diversification.

Resolving the phylogenetic position of Ombrocharis (Lamiaceae), with reference to the molecular phylogeny of tribe Elsholtzieae

Ombrocharis is the only incertae sedis genus within Lamiaceae that has not been included in a published molecular phylogenetic study. Here, we adopt a two-step approach to resolve the phylogenetic placement of the genus. Initially, the subfamilial affiliation of Ombrocharis was determined based on a combined ndhF and rbcL dataset covering all seven subfamilies of Lamiaceae. Results show that Ombrocharis is a member of Nepetoideae, a placement that is also supported by its hexacolpate pollen grains. In the second set of analyses, two nrDNA (ITS, ETS) and four cpDNA (ycf1, rps15-ycf1, trnL-F, rpl32-trnL) markers were used to explore the position of Ombrocharis within Nepetoideae. Our results demonstrate that Ombrocharis and another monotypic genus, Perillula, form a clade that is sister to the remaining genera of tribe Elsholtzieae. Ombrocharis and other taxa within Elsholtzieae share divergent stamens, a weakly 2-lipped corolla, and an asymmetric disc with an elongate anterior lobe, but it is unclear whether these features are apomorphic. This study represents both the most comprehensive phylogenetic analysis of Elsholtzieae to date and the only study to include all genera of Elsholtzieae. The monophyly of Elsholtzieae (including Ombrocharis) is well supported, and there is weak support for Elsholtzieae as sister to the rest of Nepetoideae. Additionally, our results do not support the merging of Keiskea with Collinsonia, and Elsholtzia may be polyphyletic.

Unravelling Species Relationships and Diversification within the Iconic California Floristic Province Sages (Salvia Subgenus Audibertia, Lamiaceae)

Abstract In the California Floristic Province (CA-FP) and nearby deserts, 19 species of Salvia (Lamiaceae, Mentheae) form a small radiation but an important component of the chaparral and desert communities. Traditionally, two groups within these Californian Salvia have been recognized (usually treated as sections), but relationships within each, to each other, and to other Salvia are unclear. Phylogenetic relationships of all species, with multiple accessions for most, were obtained using chloroplast DNA (cpDNA) and nuclear ribosomal DNA (nrDNA) markers. Ancestral character state reconstruction of both vegetative and floral features was done on the resulting nrDNA tree. Biogeographical analysis of the groups within the CA-FP and adjacent floristic provinces was done in BioGeoBEARS and species diversification assessed with BAMM. Significant conclusions drawn from the study include: 1) California Salvia should be classified into two monophyletic sections, Audibertia (15 species) and Echinosphace, (four species) in the new subgenus Audibertia; 2) subg. Audibertia and the Neotropical subg. Calosphace are sister clades, most closely related to Asian groups, and are likely Asian in origin; 3) nrDNA provides a fairly resolved tree for subg. Audibertia with all species monophyletic; 4) cpDNA and nrDNA trees are strongly incongruent and provide evidence that hybridization and chloroplast capture have played an important role in the evolution of subg. Audibertia; 5) ancestral character reconstruction of states in habit, possession of spines, calyx lobing, and staminal features highlights a complex (sometimes convergent) evolutionary history of this iconic CA-FP lineage; 6) subg. Audibertia arose in desert areas and more recently diversified into the southwestern California region and adjacent regions with the formation of the Mediterranean-like climate; and 7) this diversification exhibits a slight decrease in speciation and an increase in extinction rates over the groups 11 million year history.

Phylogenetic relationships, character evolution and biogeographic diversification of Pogostemon s.l. (Lamiaceae).

Pogostemon (Lamiaceae; Lamioideae) sensu lato is a large genus consisting of about 80 species with a disjunct African/Asian distribution. The infrageneric taxonomy of the genus has historically been troublesome due to morphological variability and putative convergent evolution within the genus. Notably, some species of Pogostemon are obligately aquatic, perhaps the only Lamiaceae taxa which exhibit this trait. Phylogenetic analyses using the nuclear ribosomal internal transcribed spacer (ITS) and five plastid regions (matK, rbcL, rps16, trnH-psbA, trnL-F), confirmed the monophyly of Pogostemon and its sister relationship with the genus Anisomeles. Pogostemon was resolved into two major clades, and none of the three morphologically defined subgenera of Pogostemon were supported as monophyletic. Inflorescence type (spikes with more than two lateral branches vs. a single terminal spike, or rarely with two lateral branches) is phylogenetically informative and consistent with the two main clades we recovered. Accordingly, a new infrageneric classification of Pogostemon consisting of two subgenera is proposed. Molecular dating and biogeographic diversification analyses suggest that Pogostemon split from its sister genus in southern and southeast Asia in the early Miocene. The early strengthening of the Asia monsoon system that was triggered by the uplifting of the Qinghai-Tibetan Plateau may have played an important role in the subsequent diversification of the genus. In addition, our results suggest that transoceanic long-distance dispersal of Pogostemon from Asia to Africa occurred at least twice, once in the late Miocene and again during the late-Miocene/early-Pliocene.