David Penny

Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus

Chloroplasts were once free-living cyanobacteria that became endosymbionts, but the genomes of contemporary plastids encode only ≈5–10% as many genes as those of their free-living cousins, indicating that many genes were either lost from plastids or transferred to the nucleus during the course of plant evolution. Previous estimates have suggested that between 800 and perhaps as many as 2,000 genes in the Arabidopsis genome might come from cyanobacteria, but genome-wide phylogenetic surveys that could provide direct estimates of this number are lacking. We compared 24,990 proteins encoded in the Arabidopsis genome to the proteins from three cyanobacterial genomes, 16 other prokaryotic reference genomes, and yeast. Of 9,368 Arabidopsis proteins sufficiently conserved for primary sequence comparison, 866 detected homologues only among cyanobacteria and 834 other branched with cyanobacterial homologues in phylogenetic trees. Extrapolating from these conserved proteins to the whole genome, the data suggest that ≈4,500 of Arabidopsis protein-coding genes (≈18% of the total) were acquired from the cyanobacterial ancestor of plastids. These proteins encompass all functional classes, and the majority of them are targeted to cell compartments other than the chloroplast. Analysis of 15 sequenced chloroplast genomes revealed 117 nuclear-encoded proteins that are also still present in at least one chloroplast genome. A phylogeny of chloroplast genomes inferred from 41 proteins and 8,303 amino acids sites indicates that at least two independent secondary endosymbiotic events have occurred involving red algae and that amino acid composition bias in chloroplast proteins strongly affects plastid genome phylogeny.

Branch and bound algorithms to determine minimal evolutionary trees

Abstract Two practical branch and bound algorithms for determining minimal and near-minimal phylogenetic trees from protein sequence data are presented. A mathematical description and analysis of phylogenetic trees introduces these algorithms. A comment of efficiency and fine tuning completes the paper. An example is cited where computer time was reduced from an estimated 55 days for a total search, to just under 5 minutes.

The Modern Molecular Clock

The discovery of the molecular clock — a relatively constant rate of molecular evolution — provided an insight into the mechanisms of molecular evolution, and created one of the most useful new tools in biology. The unexpected constancy of rate was explained by assuming that most changes to genes are effectively neutral. Theory predicts several sources of variation in the rate of molecular evolution. However, even an approximate clock allows time estimates of events in evolutionary history, which provides a method for testing a wide range of biological hypotheses ranging from the origins of the animal kingdom to the emergence of new viral epidemics.

The root of the mammalian tree inferred from whole mitochondrial genomes

Morphological and molecular data are currently contradictory over the position of monotremes with respect to marsupial and placental mammals. As part of a re-evaluation of both forms of data we examine complete mitochondrial genomes in more detail. There is a particularly large discrepancy in the frequencies of thymine and cytosine (T-C) between mitochondrial genomes that appears to affect some deep divergences in the mammalian tree. We report that recoding nucleotides to RY-characters, and partitioning maximum-likelihood analyses among subsets of data reduces such biases, and improves the fit of models to the data, respectively. RY-coding also increases the signal on the internal branches relative to external, and thus increases the phylogenetic signal. In contrast to previous analyses of mitochondrial data, our analyses favor Theria (marsupials plus placentals) over Marsupionta (monotremes plus marsupials). However, a short therian stem lineage is inferred, which is at variance with the traditionally deep placement of monotremes on morphological data.

Genomics and the Irreducible Nature of Eukaryote Cells

Large-scale comparative genomics in harness with proteomics has substantiated fundamental features of eukaryote cellular evolution. The evolutionary trajectory of modern eukaryotes is distinct from that of prokaryotes. Data from many sources give no direct evidence that eukaryotes evolved by genome fusion between archaea and bacteria. Comparative genomics shows that, under certain ecological settings, sequence loss and cellular simplification are common modes of evolution. Subcellular architecture of eukaryote cells is in part a physical-chemical consequence of molecular crowding; subcellular compartmentation with specialized proteomes is required for the efficient functioning of proteins.

Spectral Analysis of Phylogenetic Data

The spectral analysis of sequence and distance data is a new approach to phylogenetic analysis. For two-state character sequences, the character values at a given site split the set of taxa into two subsets, a bipartition of the taxa set. The vector which counts the relative numbers of each of these bipartitions over all sites is called a sequence spectrum. Applying a transformation called a Hadamard conjugation, the sequence spectrum is transformed to the conjugate spectrum. This conjugation corrects for unobserved changes in the data, independently from the choice of phylogenetic tree. For any given phylogenetic tree with edge weights (probabilities of state change), we define a corresponding tree spectrum. The selection of a weighted phylogenetic tree from the given sequence data is made by matching the conjugate spectrum with a tree spectrum. We develop an optimality selection procedure using a least squares best fit, to find the phylogenetic tree whose tree spectrum most closely matches the conjugate spectrum. An inferred sequence spectrum can be derived from the selected tree spectrum using the inverse Hadamard conjugation to allow a comparison with the original sequence spectrum.A possible adaptation for the analysis of four-state character sequences with unequal frequencies is considered. A corresponding spectral analysis for distance data is also introduced. These analyses are illustrated with biological examples for both distance and sequence data. Spectral analysis using the Fast Hadamard transform allows optimal trees to be found for at least 20 taxa and perhaps for up to 30 taxa.The development presented here is self contained, although some mathematical proofs available elsewhere have been omitted. The analysis of sequence data is based on methods reported earlier, but the terminology and the application to distance data are new.

Mathematical Elegance with Biochemical Realism: The Covarion Model of Molecular Evolution

There is an apparent paradox in our understanding of molecular evolution. Current biochemically based models predict that evolutionary trees should not be recoverable for divergences beyond a few hundred million years. In practice, however, trees often appear to be recovered from much older times. Mathematical models, such as those assuming that sites evolve at different rates [including a Γ distribution of rates across sites (RAS)] may in theory allow the recovery of some ancient divergences. However, such models require that each site maintain its characteristic rate over the whole evolutionary period. This assumption, however, contradicts the knowledge that tertiary structures diverge with time, invalidating the rate-constancy assumption of purely mathematical models. We report here that a hidden Markov version of the covarion model can meet both biochemical and statistical requirements for the analysis of sequence data. The model was proposed on biochemical grounds and can be implemented with only two additional parameters. The two hidden parts of this model are the proportion of sites free to vary (covarions) and the rate of interchange between fixed sites and these variable sites. Simulation results are consistent with this approach, providing a better framework for understanding anciently diverged sequences than the standard RAS models. However, a Γ distribution of rates may approximate a covarion model and may possibly be justified on these grounds. The accurate reconstruction of older divergences from sequence data is still a major problem, and molecular evolution still requires mathematical models that also have a sound biochemical basis.

Tinamous and Moa Flock Together: Mitochondrial Genome Sequence Analysis Reveals Independent Losses of Flight among Ratites

Ratites are large, flightless birds and include the ostrich, rheas, kiwi, emu, and cassowaries, along with extinct members, such as moa and elephant birds. Previous phylogenetic analyses of complete mitochondrial genome sequences have reinforced the traditional belief that ratites are monophyletic and tinamous are their sister group. However, in these studies ratite monophyly was enforced in the analyses that modeled rate heterogeneity among variable sites. Relaxing this topological constraint results in strong support for the tinamous (which fly) nesting within ratites. Furthermore, upon reducing base compositional bias and partitioning models of sequence evolution among protein codon positions and RNA structures, the tinamou-moa clade grouped with kiwi, emu, and cassowaries to the exclusion of the successively more divergent rheas and ostrich. These relationships are consistent with recent results from a large nuclear data set, whereas our strongly supported finding of a tinamou-moa grouping further resolves palaeognath phylogeny. We infer flight to have been lost among ratites multiple times in temporally close association with the Cretaceous-Tertiary extinction event. This circumvents requirements for transient microcontinents and island chains to explain discordance between ratite phylogeny and patterns of continental breakup. Ostriches may have dispersed to Africa from Eurasia, putting in question the status of ratites as an iconic Gondwanan relict taxon.

EARLY EVOLUTION: PROKARYOTES, THE NEW KIDS ON THE BLOCK

Prokaryotes are generally assumed to be the oldest existing form of life on earth. This assumption, however, makes it difficult to understand certain aspects of the transition from earlier stages in the origin of life to more complex ones, and it does not account for many apparently ancient features in the eukaryotes. From a model of the RNA world, based on relic RNA species in modern organisms, one can infer that there was an absolute requirement for a high-accuracy RNA replicase even before proteins evolved. In addition, we argue here that the ribosome (together with the RNAs involved in its assembly) is so large that it must have had a prior function before protein synthesis. A model that connects and equates these two requirements (high-accuracy RNA replicase and prior function of the ribosome) can explain many steps in the origin of life while accounting for the observation that eukaryotes have retained more vestiges of the RNA world. The later derivation of prokaryote RNA metabolism and genome structure can be accounted for by the two complementary mechanisms of r-selection and thermoreduction.

Progress with methods for constructing evolutionary trees

Evolutionists dream of a tree-reconstruction method that is efficient (fast), powerful, consistent, robust and falsifiable. These criteria are at present conflicting in that the fastest methods are weak (in their use of information in the sequences) and inconsistent (even with very long sequences they may lead to an incorrect tree). But there has been exciting progress in new approaches to tree inference, in understanding general properties of methods, and in developing ideas for estimating the reliability of trees. New phylogenetic invariant methods allow selected parameters of the underlying model to be estimated directly from sequences. There is still a need for more theoretical understanding and assistance in applying what is already known.