Evolution Is a Quantitative Science

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Evolution Is a Quantitative Science Book Review/Science in the Media Evolution Is a Quantitative Science John F. Y. Brookfield* Institute of Genetics, School of Biology, University of Nottingham, Nottingham, United Kingdom Evolutionary genetics is a mature field ing in evolutionary genetics must be of endeavour, and some of biology’s included in all bioinformatics and geno- greatest minds have contributed to the mics courses. Educators will find that theory of population genetics. Initially, foundation in Elements of Evolutionary Genet- they faced a problem, in that following the ics, by Brian and Deborah Charlesworth. rediscovery of Mendel’s results in the early This thorough and accurate textbook years of the 20th century, some saw an represents a remarkable achievement. The unbridgeable gulf between the sudden rigour of the approach is impeccable changes in appearance seen in the mutant throughout, and the text makes clear just forms of peas studied by Mendel, and the how many areas of biology, such as sex, gradual and subtle changes to evolving genome structure, migration and popula- populations envisaged by Darwin. The so- tion variation, and adaptive evolution called Neo-Darwinian synthesis linked itself, can be understood only through these ideas by considering the likely effect the application of formal models in which of Darwinian natural selection on varia- evolutionary processes are considered in a tions in Mendelian genes, variations which precise way. Most telling, however, is the would not necessarily have major effects consistently quantitative approach to data on organisms’ phenotypes. Unusually, for and their interpretation. While a full biology, this theory was developed, pri- appreciation of the book will require some marily by Fisher, Haldane and Wright, mathematical understanding, the steps prior to the existence of data sets to which required are clearly dealt with in appen- it could realistically be applied. As a result, dices, and the reader is helped by the second half of the 20th century saw Charlesworth B, Charlesworth D (2010) problems in each chapter. Elements of evolutionary genetics. evolutionary geneticists’ struggle to pro- Space precludes a full description of duce data to test theory. They were Greenwood Village, Colorado: Roberts such a major work. The focus shies away & Co. 734p ISBN (hardback) 978-0-981- especially interested in polymorphisms— from the changes to the genetic material 51942-5 US$80.00. discrete genetic variations where the rarer over long-term evolution, and methods in doi:10.1371/journal.pbio.1000381.g001 type still has an appreciable frequency in building phylogenetic trees, etc., but the population. So they studied visible rather concentrates on evolutionary causes of sex and recombination, and the polymorphisms, such as the colours and change at the genetic level over the short interpretation of genome structure in banding patterns of snails, and polymor- term, exploring how mutation, migration, population genetic terms, all of which are phisms in the charges of soluble enzymes, natural selection, and random drift shape found in the second half of the book, until, finally, abundant DNA sequence the genetic variation within and between represent areas of particular recent inter- data became available in the last years of populations and how data can give insight est. All have been investigated at the the century. into the underlying evolutionary forces theoretical level and much of this theory Now, a resurgence of interest in evolu- that are at play. Following descriptions of has been contributed by Brian and tionary genetics can be predicted, since we Deborah Charlesworth themselves. An will have, through the 1,000 genomes the measurement of genetic variation—the example is the expected, and observed, project, for example, data sets detailing theory of quantitative genetics and the evolution of sex chromosomes. If a single population genetic variation genome-wide theory of population genetics as it can be chromosome, such as the mammalian Y in many species. We need the tools of applied to infinite populations—the sam- chromosome, determines sex, its presence evolutionary genetics to describe and pling effects that create genetic drift and explain this variation. What does the determine levels of neutral variation are as a sole copy in the cell prevents it from variation tell us about population sizes in described. The expected variation be- ever undergoing recombination. The lack the past, and rates of gene flow between tween populations, the consequences and of recombination will attenuate the power subpopulations? Which parts of the ge- nome have been subject to purifying and Citation: Brookfield JFY (2010) Evolution Is a Quantitative Science. PLoS Biol 8(5): e1000381. doi:10.1371/ adaptive natural selection, and how strong journal.pbio.1000381 has this selection been? Recent advances Published May 25, 2010 in population genetic theory, in particular, Copyright: ß 2010 John F. Y. Brookfield. This is an open-access article distributed under the terms of the incorporating knowledge that chromo- Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any somes include linked sites that are subject medium, provided the original author and source are credited. to different forces such as selected versus Funding: No specific funding was received for this work. neutral sites, create powerful methods that Competing Interests: John Brookfield is an External Examiner for an MSc. course at the University of can help in answering these questions. For Edinburgh, which is the Institution which employs the authors of the book reviewed here. these and other reasons, a strong ground- * E-mail: [email protected] PLoS Biology | www.plosbiology.org 1 May 2010 | Volume 8 | Issue 5 | e1000381 of natural selection to maintain genes on determines the properties of genetic drift, values. So, for example, Fisher’s geomet- the chromosome, leading to the genetic and, with a Poisson process of mutation, rical argument considers a mutation degeneration so often seen. the complex theory of neutral genetic changing the phenotype, where the phe- But the lessons presented in this text and variation can be established on the basis notype is described by n different traits. He indeed of evolutionary genetics itself are of very simple assumptions. asks the question whether a random not restricted to students. In the 21st However, while the axioms underlying mutation is likely to move the total century there has been increasing empha- neutral variation are based on the simple phenotype in the direction of an optimum sis in the need for modelling, testing, biology, the phenotypes, including the phenotype for the environment. It turns refinement and parameter estimation in Darwinian fitness, of genotypic variants out that when the effect of the mutation is the biological sciences, as has been cap- created by mutation have irreducibly vanishingly small, the probability of a net tured by the term ‘‘systems biology.’’ complex biological causes, and, for this improvement is around half, but this drops However, it is remarkable that many reason, the incorporation of selected rapidly as the size of the mutant’s effect advocates of this approach seem unaware variation into population genetics is more increases, with the rate of decrease in- that, in evolutionary genetics, such ‘‘pre- difficult. Consequently, selective theories creasing with increasing n. From these dictive biology’’ has been the standard cannot be as precise as those involving simple premises alone can be derived a approach for decades. In the application neutrality, so selection, as a potential prediction of the quantitative relationship of a ‘‘systems’’ approach to evolutionary explanation for a particular data set, between the size of the effect of a mutation questions, a danger is that a new systems cannot easily be pitted against neutrality and the probability that it is advantageous. biology community may spend their time in a symmetrical Bayesian framework. But I don’t find myself confident that this reinventing the population genetics wheel. Rather, neutrality supplies a null hypoth- derivation, or indeed one from extreme But why has evolutionary genetics stood esis against which data can be tested, and value theory, contains enough biology to apart from biology’s resolutely qualitative, data showing the signs of selection can be likely to be correct. rather than quantitative, tradition? Most then be used as the basis of estimation of Nevertheless, biologists must get used to remarkably, while biomechanics employs selective parameters. But, if I have a the increasingly quantitative approach the laws of physics, and biochemistry is criticism of the developments in popula- that this work typifies. Biology is pervaded founded on the quantitative science of tion genetics that this new volume so by the mistaken idea that the formulation chemistry, evolutionary genetics is based admirably describes, it is that some of qualitative hypotheses, which can be on axiomatic foundations that are entirely selective models are being created axiom- resolved in a discrete unequivocal way, is biological, and yet are capable of precise atically with, my guess is, insufficient the benchmark of incisive scientific think- mathematical formulation. The rules of biological input. An example is the ing. We should embrace the idea that Mendelian genetics, encapsulated by un- prediction of the distribution of the fitness important biological answers truly come in biased inheritance and random mating in effects of advantageous new mutations, a quantitative form and that parameter a diploid genetic system, predict Hardy- where this distribution can be derived estimation from data is as important an Weinberg frequencies, the binomial sam- from Fisher’s geometrical argument or, activity in biology as it is in the other pling of gametes in finite populations more recently, from the theory of extreme sciences. PLoS Biology | www.plosbiology.org 2 May 2010 | Volume 8 | Issue 5 | e1000381.
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