Michelle M. McMahon

Inferring angiosperm phylogeny from EST data with widespread gene duplication

BackgroundMost studies inferring species phylogenies use sequences from single copy genes or sets of orthologs culled from gene families. For taxa such as plants, with very high levels of gene duplication in their nuclear genomes, this has limited the exploitation of nuclear sequences for phylogenetic studies, such as those available in large EST libraries. One rarely used method of inference, gene tree parsimony, can infer species trees from gene families undergoing duplication and loss, but its performance has not been evaluated at a phylogenomic scale for EST data in plants.ResultsA gene tree parsimony analysis based on EST data was undertaken for six angiosperm model species and Pinus, an outgroup. Although a large fraction of the tentative consensus sequences obtained from the TIGR database of ESTs was assembled into homologous clusters too small to be phylogenetically informative, some 557 clusters contained promising levels of information. Based on maximum likelihood estimates of the gene trees obtained from these clusters, gene tree parsimony correctly inferred the accepted species tree with strong statistical support. A slight variant of this species tree was obtained when maximum parsimony was used to infer the individual gene trees instead.ConclusionDespite the complexity of the EST data and the relatively small fraction eventually used in inferring a species tree, the gene tree parsimony method performed well in the face of very high apparent rates of duplication.

Phylogenomics with incomplete taxon coverage: The limits to inference

BackgroundPhylogenomic studies based on multi-locus sequence data sets are usually characterized by partial taxon coverage, in which sequences for some loci are missing for some taxa. The impact of missing data has been widely studied in phylogenetics, but it has proven difficult to distinguish effects due to error in tree reconstruction from effects due to missing data per se. We approach this problem using a explicitly phylogenomic criterion of success, decisiveness, which refers to whether the pattern of taxon coverage allows for uniquely defining a single tree for all taxa.ResultsWe establish theoretical bounds on the impact of missing data on decisiveness. Results are derived for two contexts: a fixed taxon coverage pattern, such as that observed from an already assembled data set, and a randomly generated pattern derived from a process of sampling new data, such as might be observed in an ongoing comparative genomics sequencing project. Lower bounds on how many loci are needed for decisiveness are derived for the former case, and both lower and upper bounds for the latter. When data are not decisive for all trees, we estimate the probability of decisiveness and the chances that a given edge in the tree will be distinguishable. Theoretical results are illustrated using several empirical examples constructed by mining sequence databases, genomic libraries such as ESTs and BACs, and complete genome sequences.ConclusionPartial taxon coverage among loci can limit phylogenomic inference by making it impossible to distinguish among multiple alternative trees. However, even though lack of decisiveness is typical of many sparse phylogenomic data sets, it is often still possible to distinguish a large fraction of edges in the tree.

Terraces in Phylogenetic Tree Space

Analysis of terraces in phylogenetic space can inform on phylogenetic relationships with greater computational efficiency A key step in assembling the tree of life is the construction of species-rich phylogenies from multilocus—but often incomplete—sequence data sets. We describe previously unknown structure in the landscape of solutions to the tree reconstruction problem, comprising sometimes vast “terraces” of trees with identical quality, arranged on islands of phylogenetically similar trees. Phylogenetic ambiguity within a terrace can be characterized efficiently and then ameliorated by new algorithms for obtaining a terrace’s maximum-agreement subtree or by identifying the smallest set of new targets for additional sequencing. Algorithms to find optimal trees or estimate Bayesian posterior tree distributions may need to navigate strategically in the neighborhood of large terraces in tree space.

Homoeolog-specific retention and use in allotetraploid Arabidopsis suecica depends on parent of origin and network partners

BackgroundAllotetraploids carry pairs of diverged homoeologs for most genes. With the genome doubled in size, the number of putative interactions is enormous. This poses challenges on how to coordinate the two disparate genomes, and creates opportunities by enhancing the phenotypic variation. New combinations of alleles co-adapt and respond to new environmental pressures. Three stages of the allopolyploidization process - parental species divergence, hybridization, and genome duplication - have been well analyzed. The last stage of evolutionary adjustments remains mysterious.ResultsHomoeolog-specific retention and use were analyzed in Arabidopsis suecica (As), a species derived from A. thaliana (At) and A. arenosa (Aa) in a single event 12,000 to 300,000 years ago. We used 405,466 diagnostic features on tiling microarrays to recognize At and Aa contributions to the As genome and transcriptome: 324 genes lacked Aa contributions and 614 genes lacked At contributions within As. In leaf tissues, 3,458 genes preferentially expressed At homoeologs while 4,150 favored Aa homoeologs. These patterns were validated with resequencing. Genes with preferential use of Aa homoeologs were enriched for expression functions, consistent with the dominance of Aa transcription. Heterologous networks - mixed from At and Aa transcripts - were underrepresented.ConclusionsThousands of deleted and silenced homoeologs in the genome of As were identified. Since heterologous networks may be compromised by interspecies incompatibilities, these networks evolve co-biases, expressing either only Aa or only At homoeologs. This progressive change towards predominantly pure parental networks might contribute to phenotypic variability and plasticity, and enable the species to exploit a larger range of environments.

Divergence and reticulation among montane populations of a jumping spider (Habronattus pugillis Griswold).

Populations of the jumping spider Habronattus pugillis Griswold isolated on nearby mountain ranges in southern Arizona are differentiated in many features of the males (color, shape, and orientation of setae on face; shape of carapace; markings of palpi and legs; motions during courtship behavior). These features are (mostly) consistent within a range and different between ranges. The concentration of differences in male courtship behavior and body parts exposed to the female during courtship and correlations between form and courtship behavior suggest sexual selection was involved in the differentiation. A phylogenetic analysis of the populations yields a tree that for the most part groups geographic neighbors, but the history of H. pugillis populations may not be adequately described by a tree. Geographic proximity of apparent convergences suggests that populations from at least some of the mountain ranges acquired characteristics through introgression. Lowering of the woodland habitat during the last glacial period probably brought some populations into contact, but it is not clear whether the interrange woodlands would have provided corridors for extensive mixing.

The major clades of Loasaceae: phylogenetic analysis using the plastid matK and trnL-trnF regions

Phylogenetic analyses of Loasaceae that apply DNA sequence data from the plastid trnL-trnF region and matK gene in both maximum-parsimony and maximum-likelihood searches are presented. The results place subfamily Loasoideae as the sister of a subfamily Gronovioideae-Mentzelia clade. Schismocarpus is the sister of the Loasoideae-Gronovioideae-Mentzelia clade. The Schismocarpus-Loasoideae-Gronovioideae-Mentzelia clade is the sister of Eucnide. Several clades in Loasoideae receive strong support, providing insights on generic circumscription problems. Within Mentzelia, several major clades receive strong support, which clarifies relationships among previously circumscribed sections. Prior taxonomic and phylogenetic hypotheses are modeled using topology constraints in parsimony and likelihood analyses; tree lengths and likelihoods, respectively, are compared from constrained and unconstrained analyses to evaluate the relative support for various hypotheses. We use the Shimodaira-Hasegawa (SH) test to establish the significance of the differences between constrained and unconstrained topologies. The SH test rejects topologies based on hypotheses for (1) the placement of gronovioids as the sister of the rest of Loasaceae, (2) the monophyly of subfamily Mentzelioideae as well as Gronovioideae and Loasoideae, (3) the monophyly of Loasa sensu lato as circumscribed by Urban and Gilg, and (4) the monophyly of Mentzelia torreyi and Mentzelia sect. Bartonia.

Phylogeny of Amorpheae (Fabaceae: Papilionoideae)

The legume tribe Amorpheae comprises eight genera and 240 species with variable floral form. In this study, we inferred a phylogeny for Amorpheae using DNA sequence data from the plastid trnK intron, including matK, and the nuclear ribosomal ITS1, 5.8S, and ITS2. Our data resulted in a well-resolved phylogeny in which the tribe is divided into the daleoids (Dalea, Marina, and Psorothamnus), characterized by generally papilionaceous corollas, and the amorphoids (Amorpha, Apoplanesia, Errazurizia, Eysenhardtia, and Parryella), characterized by non-papilionaceous flowers. We found evidence for the paraphyly of Psorothamnus and for the monophyly of Dalea once D. filiciformis is transferred to monophyletic Marina. Errazurizia rotundata is more closely related to Amorpha than to the other errazurizias, and Eysenhardtia is supported to be monophyletic. The monotypic Parryella and Apoplanesia are placed within the amorphoids. Among Papilionoideae, trnK/matK sequence data provide strong evidence for the monophyly of Amorpheae and place Amorpheae as sister to the recently discovered dalbergioid clade.

Exceptional reduction of the plastid genome of saguaro cactus (Carnegiea gigantea): Loss of the ndh gene suite and inverted repeat

UNLABELLED • PREMISE OF THE STUDY Land-plant plastid genomes have only rarely undergone significant changes in gene content and order. Thus, discovery of additional examples adds power to tests for causes of such genome-scale structural changes.• METHODS Using next-generation sequence data, we assembled the plastid genome of saguaro cactus and probed the nuclear genome for transferred plastid genes and functionally related nuclear genes. We combined these results with available data across Cactaceae and seed plants more broadly to infer the history of gene loss and to assess the strength of phylogenetic association between gene loss and loss of the inverted repeat (IR).• KEY RESULTS The saguaro plastid genome is the smallest known for an obligately photosynthetic angiosperm (∼113 kb), having lost the IR and plastid ndh genes. This loss supports a statistically strong association across seed plants between the loss of ndh genes and the loss of the IR. Many nonplastid copies of plastid ndh genes were found in the nuclear genome, but none had intact reading frames; nor did three related nuclear-encoded subunits. However, nuclear pgr5, which functions in a partially redundant pathway, was intact.• CONCLUSIONS The existence of an alternative pathway redundant with the function of the plastid NADH dehydrogenase-like complex (NDH) complex may permit loss of the plastid ndh gene suite in photoautotrophs like saguaro. Loss of these genes may be a recurring mechanism for overall plastid genome size reduction, especially in combination with loss of the IR.

Evolution and Development in the Amorphoid Clade (Amorpheae: Papilionoideae: Leguminosae): Petal Loss and Dedifferentiation

We used comparative developmental morphology to study the evolution of nonpapilionaceous corollas in the amorphoid clade of the tribe Amorpheae (Papilionoideae). This clade consists of five genera in which there are no papilionaceous corollas (five petals differentiated into one banner, two wing, and two keel petals). We studied the ontogenies of three nonpapilionaceous forms: corollas consisting of one petal (exemplified by Amorpha canescens), no petals (Parryella filifolia), and five petals in two types (Errazurizia megacarpa). We compared these to the ontogeny of a papilionaceous corolla (exemplified by the closely related Psorothamnus scoparius). In A. canescens, all petals initiated, but four did not grow beyond the primordial stage. In P. filifolia, no distinct petal primordia were visible. The corolla of E. megacarpa, which has only two types of petals, exhibits nonpapilionaceous characteristics at an early ontogenetic stage. Aside from the earliest primordial mounds, the petals of Psorothamnus and Errazurizia do not resemble each other, indicating that paedomorphosis is not responsible for the nonpapilionaceousness of Errazurizia. Comparing the morphological results to a phylogeny, we infer a single origin of the characteristics that differentiate Errazurizia petals from Psorothamnus petals, and we infer at least two evolutionary events leading to the reduced corolla in Parryella, Amorpha, and Errazurizia rotundata. When considered in the context of the remaining Amorpheae, in which additional floral diversification has occurred, and in the context of the entire papilionoid group, in which floral form is relatively conserved, our results indicate a relaxation of selective or developmental constraint within the clade Amorpheae.

Developmental morphology and structural homology of corolla-androecium synorganization in the tribe Amorpheae (Fabaceae: Papilionoideae)

Comparative developmental morphology was used to assess structural homology of flowers in Dalea, Marina, and Psorothamnus of the tribe Amorpheae (Fabaceae: Papilionoideae). Dalea, Marina, and some species of Psorothamnus have an unusual petal-stamen synorganization (stemonozone) in which free petals are inserted on a region that is continuous with fused stamen filaments. Developmental studies of these three genera demonstrated similarity during organogenesis. Zonal growth results in several synorganized regions, including the stemonozone of Dalea, Marina, and some Psorothamnus. Psorothamnus species that lack a stemonozone have fused stamens and free petals inserted on the hypanthium, as in most other papilionoid legumes. We concluded that the stemonozone is not strictly homologous to either androecium or receptacle, but that it is the product of a modified androecial developmental program. In the prairie clover daleas, petaloid structures positioned between the stamens have been variously interpreted as petals or as staminodes; we infer that they have an extreme form of the daleoid stemonozone, on which five petals (no staminodes) and five stamens are inserted. Assessing structural homology of these flowers allows us to characterize accurately daleoid morphology for evolutionary studies in the tribe Amorpheae.