2011-2015

Zhenxiang Xi, Liang Liu, and Charles C. Davis. 11/2015. “Genes with minimal phylogenetic information are problematic for coalescent analyses when gene tree estimation is biased.” Molecular Phylogenetics and Evolution, 92, Pp. 63-71.Abstract
The development and application of coalescent methods are undergoing rapid changes. One little explored area that bears on the application of gene-tree-based coalescent methods to species tree estimation is gene informativeness. Here, we investigate the accuracy of these coalescent methods when genes have minimal phylogenetic information, including the implementation of the multilocus bootstrap approach. Using simulated DNA sequences, we demonstrate that genes with minimal phylogenetic information can produce unreliable gene trees (i.e., high error in gene tree estimation), which may in turn reduce the accuracy of species tree estimation using gene-tree-based coalescent methods. We demonstrate that this problem can be alleviated by sampling more genes, as is commonly done in large-scale phylogenomic analyses. This applies even when these genes are minimally informative. If gene tree estimation is biased, however, gene-tree-based coalescent analyses will produce inconsistent results, which cannot be remedied by increasing the number of genes. In this case, it is not the gene-tree-based coalescent methods that are flawed, but rather the input data (i.e., estimated gene trees). Along these lines, the commonly used program PhyML has a tendency to infer one particular bifurcating topology even though it is best represented as a polytomy. We additionally corroborate these findings by analyzing the 183-locus mammal data set assembled by McCormack et al. (2012) using ultra-conserved elements (UCEs) and flanking DNA. Lastly, we demonstrate that when employing the multilocus bootstrap approach on this 183-locus data set, there is no strong conflict between species trees estimated from concatenation and gene-tree-based coalescent analyses, as has been previously suggested by Gatesy and Springer (2014).
Charles C. Davis and Zhenxiang Xi. 6/3/2015. “Horizontal gene transfer in parasitic plants.” Current Opinion in Plant Biology, 26, Pp. 14-19.Abstract

Horizontal gene transfer (HGT) between species has been a major focus of plant evolutionary research during the past decade. Parasitic plants, which establish a direct connection with their hosts, have provided excellent examples of how these transfers are facilitated via the intimacy of this symbiosis. In particular, phylogenetic studies from diverse clades indicate that parasitic plants represent a rich system for studying this phenomenon. Here, HGT has been shown to be astonishingly high in the mitochondrial genome, and appreciable in the nuclear genome. Although explicit tests remain to be performed, some transgenes have been hypothesized to be functional in their recipient species, thus providing a new perspective on the evolution of novelty in parasitic plants.

Zhenxiang Xi, Liang Liu, and Charles C. Davis. 11/15/2015. “The Impact of Missing Data on Species Tree Estimation.” Molecular Biology and Evolution, 33, 3, Pp. 838-60.Abstract

Phylogeneticists are increasingly assembling genome-scale data sets that include hundreds of genes to resolve their focal clades. Although these data sets commonly include a moderate to high amount of missing data, there remains no consensus on their impact to species tree estimation. Here, using several simulated and empirical data sets, we assess the effects of missing data on species tree estimation under varying degrees of incomplete lineage sorting (ILS) and gene rate heterogeneity. We demonstrate that concatenation (RAxML), gene-tree-based coalescent (ASTRAL, MP-EST, and STAR), and supertree (matrix representation with parsimony [MRP]) methods perform reliably, so long as missing data are randomly distributed (by gene and/or by species) and that a sufficiently large number of genes are sampled. When data sets are indecisive sensu Sanderson et al. (2010. Phylogenomics with incomplete taxon coverage: the limits to inference. BMC Evol Biol. 10:155) and/or ILS is high, however, high amounts of missing data that are randomly distributed require exhaustive levels of gene sampling, likely exceeding most empirical studies to date. Moreover, missing data become especially problematic when they are nonrandomly distributed. We demonstrate that STAR produces inconsistent results when the amount of nonrandom missing data is high, regardless of the degree of ILS and gene rate heterogeneity. Similarly, concatenation methods using maximum likelihood can be misled by nonrandom missing data in the presence of gene rate heterogeneity, which becomes further exacerbated when combined with high ILS. In contrast, ASTRAL, MP-EST, and MRP are more robust under all of these scenarios. These results underscore the importance of understanding the influence of missing data in the phylogenomics era.

Carl Veller, Martin A. Nowak, and Charles C. Davis. 7/2015. “Extended flowering intervals of bamboos evolved by discrete multiplication.” Ecology Letters, 18, Pp. 653-9.Abstract

Numerous bamboo species collectively flower and seed at dramatically extended, regular intervals - some as long as 120 years. These collective seed releases, termed 'masts', are thought to be a strategy to overwhelm seed predators or to maximise pollination rates. But why are the intervals so long, and how did they evolve? We propose a simple mathematical model that supports their evolution as a two-step process: First, an initial phase in which a mostly annually flowering population synchronises onto a small multi-year interval. Second, a phase of successive small multiplications of the initial synchronisation interval, resulting in the extraordinary intervals seen today. A prediction of the hypothesis is that mast intervals observed today should factorise into small prime numbers. Using a historical data set of bamboo flowering observations, we find strong evidence in favour of this prediction. Our hypothesis provides the first theoretical explanation for the mechanism underlying this remarkable phenomenon.

Liang Liu, Zhenxiang Xi, Shaoyuan Wu, Charles C. Davis, and Scott V. Edwards. 4/15/2015. “Estimating phylogenetic trees from genome-scale data.” Annals of the New York Academy of Sciences, 1360, Pp. 36-53.Abstract

The heterogeneity of signals in the genomes of diverse organisms poses challenges for traditional phylogenetic analysis. Phylogenetic methods known as "species tree" methods have been proposed to directly address one important source of gene tree heterogeneity, namely the incomplete lineage sorting that occurs when evolving lineages radiate rapidly, resulting in a diversity of gene trees from a single underlying species tree. Here we review theory and empirical examples that help clarify conflicts between species tree and concatenation methods, and misconceptions in the literature about the performance of species tree methods. Considering concatenation as a special case of the multispecies coalescent model helps explain differences in the behavior of the two methods on phylogenomic data sets. Recent work suggests that species tree methods are more robust than concatenation approaches to some of the classic challenges of phylogenetic analysis, including rapidly evolving sites in DNA sequences and long-branch attraction. We show that approaches, such as binning, designed to augment the signal in species tree analyses can distort the distribution of gene trees and are inconsistent. Computationally efficient species tree methods incorporating biological realism are a key to phylogenetic analysis of whole-genome data.

Charles C. Davis, Charles G. Willis, Bryan Connolly, Courtland Kelly, and Aaron M. Ellison. 10/2015. “Herbarium records are reliable sources of phenological change driven by climate and provide novel insights into species' phenological cueing mechanisms.” American Journal of Botany, 102, 10, Pp. 1599-609.Abstract

PREMISE OF THE STUDY: Climate change has resulted in major changes in the phenology of some species but not others. Long-term field observational records provide the best assessment of these changes, but geographic and taxonomic biases limit their utility. Plant specimens in herbaria have been hypothesized to provide a wealth of additional data for studying phenological responses to climatic change. However, no study to our knowledge has comprehensively addressed whether herbarium data are accurate measures of phenological response and thus applicable to addressing such questions. METHODS: We compared flowering phenology determined from field observations (years 1852-1858, 1875, 1878-1908, 2003-2006, 2011-2013) and herbarium records (1852-2013) of 20 species from New England, United States. KEY RESULTS: Earliest flowering date estimated from herbarium records faithfully reflected field observations of first flowering date and substantially increased the sampling range across climatic conditions. Additionally, although most species demonstrated a response to interannual temperature variation, long-term temporal changes in phenological response were not detectable. CONCLUSIONS: Our findings support the use of herbarium records for understanding plant phenological responses to changes in temperature, and also importantly establish a new use of herbarium collections: inferring primary phenological cueing mechanisms of individual species (e.g., temperature, winter chilling, photoperiod). These latter data are lacking from most investigations of phenological change, but are vital for understanding differential responses of individual species to ongoing climate change.

Goia M. Lyra, Emmanuelle de S. Costa, Priscilla de Jesus, Joao Carlos de Matos, Taiara A. Caires, Mariana C. Oliveira, Eurico C. Oliveira, Zhenxiang Xi, Jose Marcos de C. Nunes, and Charles C. Davis. 2015. “Phylogeny of Gracilariaceae (Rhodophyta): evidence from plastid and mitochondrial nucleotide sequences.” Journal of Phycology, 51, Pp. 356-66.Abstract

Gracilariaceae are mostly pantropical red algae and include ~230 species in seven genera. Infrafamilial classification of the group has long been based on reproductive characters, but previous phylogenies have shown that traditionally circumscribed groups are not monophyletic. We performed phylogenetic analyses using two plastid (universal plastid amplicon and rbcL) and one mitochondrial (cox1) loci from a greatly expanded number of taxa to better assess generic relationships and understand patterns of character distributions. Our analyses produce the most well-supported phylogeny of the family to date, and indicate that key characteristics of spermatangia and cystocarp type do not delineate genera as commonly suggested. Our results further indicate that Hydropuntia is not monophyletic. Given their morphological overlap with closely related members of Gracilaria, we propose that Hydropuntia be synonymized with the former. Our results additionally expand the known ranges of several Gracilariaceae species to include Brazil. Lastly, we demonstrate that the recently described Gracilaria yoneshigueana should be synonymized as G. domingensis based on morphological and molecular characters. These results demonstrate the utility of DNA barcoding for understanding poorly known and fragmentary materials of cryptic red algae.

A.M. Ellison, C. C. Davis, P. J. Calie, and R.F.C. Naczi. 2014. “Pitcher plants (Sarracenia) provide a 21st-century perspective on infraspecific ranks and interspecific hybrids: a modest proposal for appropriate recognition and usage.” Sys Bot, 39, Pp. 939-949.Abstract

Abstract—The taxonomic use of infraspecific ranks (subspecies, variety, subvariety, form, and subform), and the formal recognition of interspecific hybrid taxa, is permitted by the International Code of Nomenclature for algae, fungi, and plants. However, considerable confusion regarding the biological and systematic merits is caused by current practice in the use of infraspecific ranks, which obscures the meaningful variability on which natural selection operates, and by the formal recognition of those interspecific hybrids that lack the potential for inter-lineage gene flow. These issues also may have pragmatic and legal consequences, especially regarding the legal delimitation and management of threatened and endangered species. A detailed comparison of three contemporary floras highlights the degree to which infraspecific and interspecific variation are treated inconsistently. An in-depth analysis of taxonomy of the North American flowering plant genus Sarracenia (Sarraceniaceae) provides an ideal case study illustrating the confusion that can arise from inconsistent and apparently arbitrary designation of infraspecific ranks and hybrid taxa. To alleviate these problems, we propose the abandonment of infraspecific ranks of “variety” and “form,” and discourage naming of sterile interspecific hybrids except for use in the horticultural or agronomic trade. Our recommendations for taxonomic practice are in accord with the objectives proposed in the Systematics Agenda 2000, Systematics Agenda 2020, and the Global Strategy for Plant Conservation. Keywords—Flora, nomenclature, Sarracenia, species concept, systematics.

Bojian Zhong, Zhaoxiang Xi, Vadim V. Goremykin, Richard Fong, Patricia A. McLenachan, Philip M. Novis, Charles C. Davis, and David Penny. 2014. “Streptophyte algae and the origin of land plants revisited using heterogeneous models with three new algal chloroplast genomes.” Molecular Biology and Evolution, 31, 1, Pp. 177-183.Abstract
The phylogenetic branching order of the green algal groups that gave rise to land plants remains uncertain despite its fundamental importance to understanding plant evolution. Previous studies have demonstrated that land plants evolved from streptophyte algae, but different lineages of streptophytes have been suggested to be the sister group of land plants. To better understand the evolutionary history of land plants and to determine the potential effects of “long-branch attraction” in phylogenetic reconstruction, we analyzed a chloroplast genome data set including three new chloroplast genomes from streptophyte algae: Coleochaetae orbicularis (Coleochaetales), Nitella hookeri (Charales), and Spirogyra communis (Zygnematales). We further applied a site pattern sorting method together with site- and time-heterogeneous models to investigate the branching order among streptophytes and land plants. Our chloroplast phylogenomic analyses support previous hypotheses based on nuclear data in placing Zygnematales alone, or a clade consisting of Coleochaetales plus Zygnematales, as the closest living relatives of land plants.
Whenzing Zhang, V.ictorW. Steinmann, Lachezar Nikolov, Elena M. Kramer, and Charles C. Davis. 2014. “Divergent genetic mechanisms underlie reversals to radial floral symmetry from diverse zygomorphic flowered ancestors.” Frontiers in Plant Science, 4, 302, Pp. 1-13.Abstract
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.
L.achezar A. Nikolov, Yost M. Staedler, Sugumaram Manickam, Jurg Schonenberger, Peter K. Endress, Elena M. Kramer, and Charles C. Davis. 2014. “Floral structure and development in Rafflesiaceae with emphasis on their exceptional gynoecia.” American Journal of Botany, 101, 2, Pp. 225-43.Abstract

PREMISE OF THE STUDY: The holoparasitic plant family Rafflesiaceae include the world's largest flowers. Despite their iconic status, relatively little is known about the morphology and development of their flowers. A recent study clarified the organization of the outer (sterile) floral organs, surprisingly revealing that their distinctive floral chambers arose via different developmental pathways in the two major genera of the family. Here, we expand that research to investigate the structure and development of the reproductive organs of Rafflesiaceae. METHODS: Serial sectioning, scanning electron microscopy, and x-ray tomography of floral buds were employed to reconstruct the structure and development of all three Rafflesiaceae genera. KEY RESULTS: Unlike most angiosperms, which form their shoot apex from the primary morphological surface, the shoot apex of Rafflesiaceae instead forms secondarily via internal cell separation (schizogeny) along the distal boundary of the host-parasite interface. Similarly, the radially directed ovarial clefts of the gynoecium forms via schizogeny within solid tissue, and no carpels are initiated from the floral apex. CONCLUSIONS: The development of the shoot apex and gynoecium of Rafflesiaceae are highly unusual. Although secondary formation of the morphological surface from the shoot apex has been documented in other plant groups, secondary derivation of the inner gynoecium surface is otherwise unknown. Both features are likely synapomorphies of Rafflesiaceae. The secondary derivation of the shoot apex may protect the developing floral shoot as it emerges from within dense host tissue. The secondary formation of the ovarial clefts may generate the extensive placental area necessary to produce hundreds of thousands of ovules.

L. P. Lagomarsino, A. Antonelli, N. Muchhala, A. Timmermann, S. Mathews, and C. C. Davis. 2014. “Phylogeny, classification, and fruit evolution of the species-rich Neotropical bellflowers (Campanulaceae: Lobelioideae).” Am J Bot, 101, Pp. 2097-112.Abstract

* PREMISE OF THE STUDY: The species-rich Neotropical genera Centropogon, Burmeistera, and Siphocampylus represent more than half of the approximately 1200 species in the subfamily Lobelioideae (Campanulaceae). They exhibit remarkable morphological variation in floral morphology and habit. Limited taxon sampling and phylogenetic resolution, however, obscures our understanding of relationships between and within these genera and underscores our uncertainty of the systematic value of fruit type as a major diagnostic character.* METHODS: We inferred a phylogeny from five plastid DNA regions (rpl32-trnL, ndhF-rpl32, rps16-trnK, trnG-trnG-trns, rbcL) using maximum-likelihood and Bayesian inference. Ancestral character reconstructions were applied to infer patterns of fruit evolution.* KEY RESULTS: Our results demonstrate that the majority of species in the genera Centropogon, Burmeistera, and Siphocampylus together form a primarily mainland Neotropical clade, collectively termed the "centropogonids." Caribbean Siphocampylus, however, group with other Caribbean lobelioid species. We find high support for the monophyly of Burmeistera and the polyphyly of Centropogon and mainland Siphocampylus. The ancestral fruit type of the centropogonids is a capsule; berries have evolved independently multiple times.* CONCLUSIONS: Our plastid phylogeny greatly improves the phylogenetic resolution within Neotropical Lobelioideae and highlights the need for taxonomic revisions in the subfamily. Inference of ancestral character states identifies a dynamic pattern of fruit evolution within the centropogonids, emphasizing the difficulty of diagnosing broad taxonomic groups on the basis of fruit type. Finally, we identify that the centropogonids, Lysipomia, and Lobelia section Tupa form a Pan-Andean radiation with broad habitat diversity. This clade is a prime candidate for investigations of Neotropical biogeography and morphological evolution.

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