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The Origin and Evolution of Model Organisms

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The Origin and Evolution of Model Organisms REVIEWS THE ORIGIN AND EVOLUTION OF MODEL ORGANISMS S. Blair Hedges The phylogeny and timescale of life are becoming better understood as the analysis of genomic data from model organisms continues to grow. As a result, discoveries are being made about the early history of life and the origin and development of complex multicellular life. This emerging comparative framework and the emphasis on historical patterns is helping to bridge barriers among organism-based research communities. Model organisms represent only a small fraction of the these species are receiving an unusually large amount of biodiversity that exists on Earth, although the research attention from the research community and fall under that has resulted from their study forms the core of bio- the broad definition of “model organism”. logical knowledge. Historically, research communities Knowledge of the relationships and times of origin of — often in isolation from one another — have focused these species can have a profound effect on diverse areas on these model organisms to gain an insight into the of research2. For example, identifying the closest relatives general principles that underlie various disciplines, such of a disease vector will help to decipher unique traits — as genetics, development and evolution. This has such as single-nucleotide polymorphisms — that might changed in recent years with the availability of complete contribute to a disease phenotype. Similarly, knowing genome sequences from many model organisms, which that our closest relative is the chimpanzee is crucial for has greatly facilitated comparisons between the different identifying genetic changes in coding and regulatory species and increased interactions among organism- genomic regions that are unique to humans, and are based research communities. All fields have benefited possibly associated with traits such as intelligence3. from these advances, including evolutionary biology, in Furthermore, knowing when humans and chimpanzees which the surge in molecular data has greatly clarified diverged from one another allows researchers to calibrate estimates of phylogenetic relationships and divergence the rates of genetic change in modern humans and to times among taxa. estimate when populations migrated to different regions In past decades, the term “model organism” has been of the World4. In addition, genomic comparisons across narrowly applied to those species — such as mouse or species are fundamental to locating conserved gene Drosophila — that, because of their small size and short sequences, which presumably reflect the constraints that generation times, facilitate experimental laboratory are imposed by natural selection5. The methodology for research. However, in the past decade, with the increase generating phylogenetic trees from sequence data con- in the number of genome-sequencing projects, this defi- tinues to be refined and expanded, and aids the above nition has broadened. For example, researchers have studies. The various methods that are, at present, used to focused attention on some organisms, such as the tiger generate phylogenetic trees and estimate divergence NASA Astrobiology Institute pufferfish, because of unique aspects of their genome times among taxa are described in BOX 1. and Department of Biology, rather than their feasibility for experimental studies, and Model organisms are found among the prokaryotes, 208 Mueller Laboratory, referred to them as “genomic” models1. In most cases, protists, fungi, plants and animals. Therefore, a discus- The Pennsylvania State economics has had a large part in the choice of organ- sion of their origin and evolution necessarily concerns University, University Park, Pennsylvania 16802, USA. ism to study, such as the agriculturally important species the pattern and timing of the “tree of life”.In the early e-mail: [email protected] (for example, rice) and those related to human health 1990s, the tree of life was derived mostly from the small doi:10.1038/nrg929 (for example, the malarial parasite Plasmodium). All subunit ribosomal RNA (rRNA) gene6, and the timescale 838 | NOVEMBER 2002 | VOLUME 3 www.nature.com/reviews/genetics © 2002 Nature Publishing Group REVIEWS was on the basis of the geochemical and fossil record7,8 fusion of some evolutionary branches. The relative con- (FIG. 1a). Eukaryotes and their genomes were considered tribution of these major gene transfers, other HORIZONTAL to be closest relatives in the Archaebacteria (and their TRANSFER events and the number of symbiotic events is genomes), just as any two species might be close relatives. highly debated9, with some favouring the existence of a The current view (FIG. 1b) is noticeably different, and it eukaryotic root10. The times of divergence — as esti- holds that eukaryotes are genomic hybrids of Eubacteria mated from molecular clocks (FIG. 1c; BOX 1) — are also and Archaebacteria: numerous genes were transferred to debated, generating attention because they are often the eukaryote nucleus during symbiotic events, such as older than the corresponding fossil dates. However, this those that gave rise to mitochondria, leading to the is not surprising as fossil-based times are minimum Box 1 | Methods for estimating molecular phylogenies and times of divergence Sequence data a Both DNA and protein sequences are used for Calibration time (to determine rate) estimating phylogenetic relationships and times of Unknown time = d(sp. 1 vs sp. 2) / (rate) divergence among taxa. Typically, DNA sequences Species 1 are used for relatively recent events — for example, HORIZONTAL TRANSFER the human and chimpanzee split — when protein Species 2 The transfer of genetic material sequences are too conserved to be useful. Protein Species 3 between the genomes of two sequences are desirable for more ancient events — organisms, which are usually for example, human divergence from insects — Species 4 different species. when DNA sequences are usually too divergent to Time NEIGHBOUR JOINING make accurate estimates on the basis of patterns of nucleotide substitutions. Unequal base or amino- A method that selects the tree b that has the shortest overall acid composition among the genomes of different True rate (unknown) length (sum of all branch species is common and makes sequence change more Best rate lengths). difficult to estimate. In addition, sequence length is a limiting factor, in that the average gene (coding) or Average rate MAXIMUM LIKELIHOOD Time (underestimate) A method that selects the tree protein sequence (~1,000 nucleotides, ~350 amino (fossil record) that has the highest probability acids) is usually not long enough to yield a robust of explaining the sequence data, phylogeny or time estimate, and therefore many Sequence divergence under a specific model of genes and proteins must be used. substitution (changes in the c Speciation event nucleotide or amino-acid Phylogeny estimation (orthology) sequence). The general principle behind phylogenetic methods Species 1 Gene 1 is to find a tree that minimizes sequence change. For Gene duplication Species 2 BAYESIAN METHOD example, if two species have a unique amino acid at a (paralogy) Species 1 Gene 2 A method that selects the tree particular site and are joined in the tree, only one Species 2 that has the greatest posterior Species 1 probability (probability that the change (in their ancestor) is needed to explain this Gene 3 Species 2 tree is correct), under a specific data. Conversely, an additional change would be model of substitution. required if the two species were not joined in the Time tree, making the other tree less likely to be the true MAXIMUM PARSIMONY tree. The two tree-building methods that are most A method that selects the tree often used with molecular sequence data are minimum evolution, such as NEIGHBOUR JOINING, and MAXIMUM LIKELIHOOD117. that requires the fewest number 118 of substitutions. These methods, and the BAYESIAN METHOD , are flexible enough to include diverse information on the biological nature of molecular sequence change, such as rate variation among sites. A fourth method, MAXIMUM PARSIMONY, is also widely used. BOOTSTRAP METHOD Although the various methods are quite different from one another, they often result in the same phylogenetic tree. As applied to molecular Reliability can be tested in different ways, with the BOOTSTRAP METHOD119 being the most widely used. Phylogeneticists often phylogenies. Nucleotide or use and compare several methods in a single study to evaluate the robustness of their results. amino-acid sites are sampled randomly, with replacement, Time estimation and a new tree is constructed. On the basis of the observation that sequences diverge in a roughly clock-like fashion, the ‘molecular clock’ method is This is repeated many times and used to estimate divergence time120. Usually, the rate of divergence is determined by dividing the substitutional the frequency of appearance of a differences observed between two species, by the time elapsed since their divergence. This is based on a fossil calibration, particular node among the with the ‘calibration time’ for the divergence of species 1 and 2 being shown in . The rate obtained is then used to bootstrap trees is viewed as a a support (confidence) value for estimate the timing of unknown branch points on the tree (a). Divergence times that are based on fossils always yield deciding on the significance of overestimates of the true rates, so the measuring of one or a few robust calibration points might be more reliable
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