Coalescent theory
Coalescent theory is a model of how gene variants sampled from a population may have originated from a common ancestor. In the simplest case, coalescent theory assumes no recombination, no natural selection, and no gene flow or population structure, meaning that each variant is equally likely to have been passed from one generation to the next. The model looks backward in time, merging alleles into a single ancestral copy according to a random process in coalescence events. Under this model, the expected time between successive coalescence events increases almost exponentially back in time. Variance in the model comes from both the random passing of alleles from one generation to the next, and the random occurrence of mutations in these alleles.
The mathematical theory of the coalescent was developed independently by several groups in the early 1980s as a natural extension of classical population genetics theory and models, but can be primarily attributed to John Kingman. Advances in coalescent theory include recombination, selection, overlapping generations and virtually any arbitrarily complex evolutionary or demographic model in population genetic analysis.
The model can be used to produce many theoretical genealogies, and then compare observed data to these simulations to test assumptions about the demographic history of a population. Coalescent theory can be used to make inferences about population genetic parameters, such as migration, population size and recombination.
Theory
Time to coalescence
Consider a single gene locus sampled from two haploid individuals in a population. The ancestry of this sample is traced backwards in time to the point where these two lineages coalesce in their most recent common ancestor. Coalescent theory seeks to estimate the expectation of this time period and its variance.The probability that two lineages coalesce in the immediately preceding generation is the probability that they share a parental DNA sequence. In a population with a constant effective population size with 2Ne copies of each locus, there are 2Ne "potential parents" in the previous generation. Under a random mating model, the probability that two alleles originate from the same parental copy is thus 1/ and, correspondingly, the probability that they do not coalesce is 1 − 1/.
At each successive preceding generation, the probability of coalescence is geometrically distributed—that is, it is the probability of noncoalescence at the t − 1 preceding generations multiplied by the probability of coalescence at the generation of interest:
For sufficiently large values of Ne, this distribution is well approximated by the continuously defined exponential distribution
This is mathematically convenient, as the standard exponential distribution has both the expected value and the standard deviation equal to 2Ne. Therefore, although the expected time to coalescence is 2Ne, actual coalescence times have a wide range of variation. Note that coalescent time is the number of preceding generations where the coalescence took place and not calendar time, though an estimation of the latter can be made multiplying 2Ne with the average time between generations. The above calculations apply equally to a diploid population of effective size Ne. Some effectively haploid DNA elements, such as mitochondrial DNA, however, are only carried by one sex, and therefore have one quarter the effective size of the equivalent diploid population
Neutral variation
Coalescent theory can also be used to model the amount of variation in DNA sequences expected from genetic drift and mutation. This value is termed the mean heterozygosity, represented as. Mean heterozygosity is calculated as the probability of a mutation occurring at a given generation divided by the probability of any "event" at that generation. The probability that the event is a mutation is the probability of a mutation in either of the two lineages:. Thus the mean heterozygosity is equal toFor, the vast majority of allele pairs have at least one difference in nucleotide sequence.
Graphical representation
Coalescents can be visualised using dendrograms which show the relationship of branches of the population to each other. The point where two branches meet indicates a coalescent event.Applications
Disease gene mapping
The utility of coalescent theory in the mapping of disease is slowly gaining more appreciation; although the application of the theory is still in its infancy, there are a number of researchers who are actively developing algorithms for the analysis of human genetic data that utilise coalescent theory.A considerable number of human diseases can be attributed to genetics, from simple Mendelian diseases like sickle-cell anemia and cystic fibrosis, to more complicated maladies like cancers and mental illnesses. The latter are polygenic diseases, controlled by multiple genes that may occur on different chromosomes, but diseases that are precipitated by a single abnormality are relatively simple to pinpoint and trace – although not so simple that this has been achieved for all diseases. It is immensely useful in understanding these diseases and their processes to know where they are located on chromosomes, and how they have been inherited through generations of a family, as can be accomplished through coalescent analysis.
Genetic diseases are passed from one generation to another just like other genes. While any gene may be shuffled from one chromosome to another during homologous recombination, it is unlikely that one gene alone will be shifted. Thus, other genes that are close enough to the disease gene to be linked to it can be used to trace it.
Polygenic diseases have a genetic basis even though they don't follow Mendelian inheritance models, and these may have relatively high occurrence in populations, and have severe health effects. Such diseases may have incomplete penetrance, and tend to be polygenic, complicating their study. These traits may arise due to many small mutations, which together have a severe and deleterious effect on the health of the individual.
Linkage mapping methods, including Coalescent theory can be put to work on these diseases, since they use family pedigrees to figure out which markers accompany a disease, and how it is inherited. At the very least, this method helps narrow down the portion, or portions, of the genome on which the deleterious mutations may occur. Complications in these approaches include epistatic effects, the polygenic nature of the mutations, and environmental factors. That said, genes whose effects are additive carry a fixed risk of developing the disease, and when they exist in a disease genotype, they can be used to predict risk and map the gene. Both regular the coalescent and the shattered coalescent have been put to work in understanding disease genes.
Studies have been carried out correlating disease occurrence in fraternal and identical twins, and the results of these studies can be used to inform coalescent modeling. Since identical twins share all of their genome, but fraternal twins only share half their genome, the difference in correlation between the identical and fraternal twins can be used to work out if a disease is heritable, and if so how strongly.
The genomic distribution of heterozygosity
The human single-nucleotide polymorphism map has revealed large regional variations in heterozygosity, more so than can be explained on the basis of random chance. In part, these variations could be explained on the basis of assessment methods, the availability of genomic sequences, and possibly the standard coalescent population genetic model. Population genetic influences could have a major influence on this variation: some loci presumably would have comparatively recent common ancestors, others might have much older genealogies, and so the regional accumulation of SNPs over time could be quite different. The local density of SNPs along chromosomes appears to cluster in accordance with a variance to mean power law and to obey the Tweedie compound Poisson distribution. In this model the regional variations in the SNP map would be explained by the accumulation of multiple small genomic segments through recombination, where the mean number of SNPs per segment would be gamma distributed in proportion to a gamma distributed time to the most recent common ancestor for each segment.History
Coalescent theory is a natural extension of the more classical population genetics concept of neutral evolution and is an approximation to the Fisher–Wright model for large populations. It was discovered independently by several researchers in the 1980s.Software
A large body of software exists for both simulating data sets under the coalescent process as well as inferring parameters such as population size and migration rates from genetic data.- – Bayesian inference package via MCMC with a wide range of coalescent models including the use of temporally sampled sequences.
- – software package for inferring phylogeny and divergence times among populations under a multispecies coalescent process.
- – software for simulating genetic data under the coalescent model.
- – a user-friendly approach to ABC for inference on population history using molecular markers.
- – a Python library for phylogenetic computing, with classes and methods for simulating pure coalescent trees as well as constrained coalescent trees under the multispecies coalescent model.
- – software for the fine-scale mapping of linkage disequilibrium mapping of disease genes using coalescent theory based on a Bayesian MCMC framework.
- software for estimation of population genetics parameters using coalescent theory and simulation. See also
- – rapid coalescent-based whole-genome simulation
- – a computer package for the simulation of genotypic data under general isolation by distance models.
- – IMa implements the same Isolation with Migration model, but does so using a new method that provides estimates of the joint posterior probability density of the model parameters. IMa also allows log likelihood ratio tests of nested demographic models. IMa is based on a method described in Hey and Nielsen. IMa is faster and better than IM, and it can be used for most of the situations and options that IM can be used for.
- – software for estimation of rates of population growth, migration, and recombination.
- – a program which implements coalescent algorithms for a maximum likelihood analysis of genetic data with a focus on spatially structured populations.
- – maximum likelihood and Bayesian inference of migration rates under the n-coalescent. The inference is implemented using MCMC
- – Markovian Coalescent Simulator – simulates genealogies spatially across chromosomes as a Markovian process. Similar to the SMC algorithm of McVean and Cardin, and supports all demographic scenarios found in Hudson's ms.
- – Richard Hudson's original program for generating samples under neutral models and an extension which allows recombination hotspots.
- – an extended version of ms that includes selective sweeps.
- – a fast and scalable ms-compatible simulator, allowing demographic simulations, producing compact output files for thousands or millions of genomes.
- – software to simulate coding sequences with inter/intracodon recombination, migration, growth rate and longitudinal sampling.
- – software to simulate nucleotide, coding and amino acid sequences under the coalescent with demographics, recombination, population structure with migration and longitudinal sampling.
- – structure Ancestral Recombination Graph by Magnus Nordborg
- – software to simulate genetic data under the coalescent model with complex demography and recombination
- – forward simulation software allowing sampling of genealogies and data sets under diverse selective and demographic models.
Articles
- Arenas, M. and Posada, D. Simulation of Genome-Wide Evolution under Heterogeneous Substitution Models and Complex Multispecies Coalescent Histories.
- Arenas, M. and Posada, D. Recodon: Coalescent simulation of coding DNA sequences with recombination, migration and demography.
- Arenas, M. and Posada, D. Coalescent simulation of intracodon recombination.
- Browning, S.R. Multilocus association mapping using variable-length markov chains.
- Cornuet J.-M., Pudlo P., Veyssier J., Dehne-Garcia A., Gautier M., Leblois R., Marin J.-M., Estoup A. DIYABC v2.0: a software to make Approximate Bayesian Computation inferences about population history using Single Nucleotide Polymorphism, DNA sequence and microsatellite data.
- Degnan, JH and LA Salter. 2005. Gene tree distributions under the coalescent process. Evolution 59: 24–37.
- Donnelly, P., Tavaré, S. Coalescents and genealogical structure under neutrality. Annual Review of Genetics 29:401-421
- Ewing, G. and Hermisson J., MSMS: a coalescent simulation program including recombination, demographic structure and selection at a single locus,
- Hellenthal, G., Stephens M. msHOT: modifying Hudson's ms simulator to incorporate crossover and gene conversion hotspots
- Hudson RR Properties of a neutral allele model with intragenic recombination. Theoretical Population Biology 23:183-201.
- Hudson RR Oxford Surveys in Evolutionary Biology 7: 1-44
- Hudson RR Generating samples under a Wright-Fisher neutral model.
- Kendal WS An exponential dispersion model for the distribution of human single nucleotide polymorphisms. Mol Biol Evol 20: 579-590
- Hein, J., Schierup, M., Wiuf C. Gene Genealogies, Variation and Evolution: A Primer in Coalescent Theory Oxford University Press
- Kaplan, N.L., Darden, T., Hudson, R.R. The coalescent process in models with selection. Genetics 120:819-829
- Kingman, J.F.C. Origins of the coalescent 1974-1982.
- Leblois R., Estoup A. and Rousset F. IBDSim: a computer program to simulate genotypic data under isolation by distance
- Liang L., Zöllner S., Abecasis G.R. GENOME: a rapid coalescent-based whole genome simulator. Bioinformatics
- Mailund, T., Schierup, M.H., Pedersen, C.N.S., Mechlenborg, P. J. M., Madsen, J.N., Schauser, L. CoaSim: A Flexible Environment for Simulating Genetic Data under Coalescent Models
- Möhle, M., Sagitov, S. A classification of coalescent processes for haploid exchangeable population models The Annals of Probability 29:1547-1562
- Morris, A. P., Whittaker, J. C., Balding, D. J. Fine-scale mapping of disease loci via shattered coalescent modeling of genealogies
- Neuhauser, C., Krone, S.M. The genealogy of samples in models with selection
- Pitman, J. Coalescents with multiple collisions The Annals of Probability 27:1870-1902
- Harding, Rosalind, M. 1998. New phylogenies: an introductory look at the coalescent. pp. 15–22, in Harvey, P. H., Brown, A. J. L., Smith, J. M., Nee, S. New uses for new phylogenies. Oxford University Press
- Rosenberg, N.A., Nordborg, M. Genealogical Trees, Coalescent Theory and the Analysis of Genetic Polymorphisms. Nature Reviews Genetics 3:380-390
- Sagitov, S. The general coalescent with asynchronous mergers of ancestral lines Journal of Applied Probability 36:1116-1125
- Schweinsberg, J. Coalescents with simultaneous multiple collisions Electronic Journal of Probability 5:1-50
- Slatkin, M. Simulating genealogies of selected alleles in populations of variable size Genetic Research 145:519-534
- Tajima, F. Evolutionary Relationship of DNA Sequences in finite populations. Genetics 105:437-460
- Tavare S, Balding DJ, Griffiths RC & Donnelly P. 1997. Inferring coalescent times from DNA sequence data. Genetics 145: 505-518.
- The international SNP map working group. 2001. A map of human genome variation containing 1.42 million single nucleotide polymorphisms. Nature 409: 928-933.
- Zöllner S. and Pritchard J.K. Coalescent-Based Association Mapping and Fine Mapping of Complex Trait Loci
- Rousset F. and Leblois R. Likelihood and Approximate Likelihood Analyses of Genetic Structure in a Linear Habitat: Performance and Robustness to Model Mis-Specification
Books
- Hein, J; Schierup, M. H., and Wiuf, C. Gene Genealogies, Variation and Evolution - A Primer in Coalescent Theory. Oxford University Press, 2005..
- Nordborg, M.
- Chapter 7 in Balding, D., Bishop, M., Cannings, C., editors, Handbook of Statistical Genetics. Wiley
- Wakeley J. An Introduction to Coalescent Theory Roberts & Co
- Rice SH.. Evolutionary Theory: Mathematical and Conceptual Foundations. Sinauer Associates: Sunderland, MA. See esp. ch. 3 for detailed derivations.
- Berestycki N. "Recent progress in coalescent theory" 2009 ENSAIOS Matematicos vol.16
- Bertoin J. "Random Fragmentation and Coagulation Processes"., 2006. Cambridge Studies in Advanced Mathematics, 102. Cambridge University Press, Cambridge, 2006. ;
- Pitman J. "Combinatorial stochastic processes" Springer