Review of : Charlesworth, B. and Charlesworth D. 2010 . Elements of Evolutionary Genetics . Roberts and Company Publishers . 768 pp. ISBN : 9780981519425 ; $80.00 HB .

Elements of Evolutionary Genetics is the new book by Brian and Deborah Charlesworth. Over the last three plus decades, the Charlesworths have worked on problems theoretical and empirical, advancing our understanding of phenotypic and molecular evolution in both plant and animal systems. The number and quality of their contributions is staggering. It would be difficult to imagine two more qualified individuals to write such a book.

Their text covers a wide range of topics from classic (phenotypic) issues such as mutation load and mating system evolution to more modern (molecular) problems such as coalescence in subdivided populations and inferences from allele frequency spectra.

As with their research, their book is deeply rooted in theory. A substantial fraction of every chapter consists of key theoretical results, typically along with the derivation itself (or a skeleton version thereof), and some discussion of the model's assumptions and implications. Empirical data are discussed at length in a few sections but, in most cases, examples are only briefly mentioned or simply cited. The emphasis of the book is on exposing the reader to the relevant theory rather than providing a comprehensive review of empirical results.

Unsurprisingly, this book contains many of the same topics covered by two other recent population genetics texts (Genetics of Populations, 3rd ed., by P. W. Hedrick (2005) and Principles of Population Genetics, 4th ed., by D. L. Hartl and A. G. Clark (2007)). In comparison to those books, the Charlesworths’ text is pitched at a somewhat higher level on average and with a heavier emphasis on the theory. Of course, the overlap among the three books is far from complete and even in the areas of common ground there is fair bit of among-book variation in the depth and style of coverage given to different topics.

Each chapter of the Charlesworths’ text opens with a very useful summary in which they clearly outline what will be covered and highlight the most important results. Each such summary ends with a fantastic quote or two from luminary figures of our field such Darwin, Wright, and Haldane, epitomizing their great insights. An amusing exception is the chapter discussing the importance of genetic drift that includes an elegant quote from the Bible on the power of chance events occurring over time. This is juxtaposed with the following quote from R. A. Fisher (1930): “The very small range of selective intensity in which a factor may be regarded as effectively neutral suggests that such a condition must in general be extremely transient.” Of course, Fisher gets his due in many other sections.

The opening chapter discusses various forms of genetic variation and ways in which it can be measured and quantitatively described. This is relatively dry material but is made more interesting by the inclusion of little snippets of history. Here they identify the limitations of classical and quantitative genetic techniques in solving traditional problems (such as the mechanisms maintaining genetic variance in fitness) that motivated the pursuit of more molecular-level approaches. From this perspective, it is interesting to consider what we have and have not yet learned in this era of sequence data. While we have learned much about problems barely conceived when evolutionary biologists first began studying variation at the molecular level (e.g., evolution of GC content, transposable element abundance, recombination hotspots), some of the classic problems that motivated the original pursuit of molecular methods remain largely unanswered.

Chapters 2–5 cover a number of classic issues in population genetics including basic selection theory, mutation-selection balance, effective population size, and diffusion approximations for studying mutation and selection in finite populations. I particularly enjoyed the review of the models for the maintenance of genetic variance in fitness through balancing selection (Chapter 2). Simplified versions of the classic models are presented and connections between various models are discussed. Although this topic is currently somewhat out of vogue, the maintenance of genetic variation is a major problem in evolutionary biology that has never been satisfactorily resolved. Chapter 4 returns to this topic in presenting mutation-selection balance. After discussing the classic theory, the Charlesworths review how this theory can be modified to make empirically testable predictions using quantitative genetics. The available data, which is sadly limited to Drosophila melanogaster, suggest that mutation-selection balance may be able to account for at most half of the genetic variation in viability.

Another highlight for me was the section on the genetics of adaptation. This begins with a concise but clear discussion of Fisher's classic geometric model of adaptation. This includes a description of major advances to this theory that have occurred in the last decade or so; these advances have revitalized the field so it was nice to see their inclusion here. This is followed by a discussion of sequence-based models and their results. Although this material is also presented clearly, it would have been helpful to provide a direct comparison of the phenotypic and sequence-based perspectives. Some empirical results from QTL mapping and experimental evolution supporting the predictions of the landscape models are presented. As they do elsewhere in the book, the Charlesworths remind us of some of the key assumptions underlying the models, which in this case is the assumption of a single fitness peak. They discuss how different predictions would be expected when multiple fitness peaks occur and offer as a case study the Batesian mimetic butterflies that adorn the book's front cover.

In introducing effective population size, the Charlesworths’ book uses a different approach than is typical. True novices may find their verbal description of Ne too brief to grasp but I suspect that most readers of this book would already have some familiarity with the concept. Moreover, the Charlesworths do not follow the textbook tradition of using variance- or inbreeding-based approaches to demonstrate how violations of “idealism” (e.g., biased sex ratios, non-Poisson variances) alter effective population sizes. Rather they launch directly into a coalescent-based approach. Although this is initially more difficult to follow than the traditional presentations, this approach is more powerful as the authors show how it can be used to calculate Ne in a wide variety of circumstances, including different modes of inheritance.

The middle section of the book, Chapters 6–8, focuses on material that is at the heart of modern molecular population genetics. It begins with a reasonably standard presentation of neutral theory and its predictions and this leads into various classic tests of molecular evolution. This is followed by a description of recent advances such as estimation of the fraction of fixed differences due to beneficial mutations (α) and estimating the intensity of purifying selection (Nes). The Charlesworths show how theory provides a framework to allow such estimation but they also describe how violations of the assumptions of the underlying theory can lead to biased estimates. The limits and potential biases of these methods is an important message for those new to the field as it is easy to become seduced by the apparent sophistication of these types of approaches. Newcomers to the field will also need to know likelihood and/or Bayesian techniques to use these methods but, unfortunately, little instruction is given in this regard. I suspect that the book would be more useful to students had it supplied a few, more thoroughly explained examples of how to employ likelihood and Bayesian techniques in these types of contexts. Similarly, coalescent simulations, which are important for other topics in the book, are briefly described but their use in combination with likelihood methods is not explained.

Chapter 7 deals with the notoriously difficult subject of coalescence in structured populations. The authors present model results for some theoretically simple scenarios such as the island model and then describe results from more complex theory. They are able to provide some insights into why certain approximations seem to yield relatively robust results but their coverage of these issues is necessarily quite limited. The recent book on coalescent theory by Wakeley (2008) is heavily cited throughout this chapter and students deeply interested in this subject will likely need to read that text to fully understand this subject. Nonetheless, the Charlesworths lay out the key issues (and caveats) and provide a useful introduction to this challenging subject.

Chapter 8 focuses on issues revolving around linkage. This begins with a discussion of linkage disequilibrium and the factors affecting disequilibrium between neutral sites including recombination, mating system, population structure, and drift. This is followed by a discussion of the effect of selection on patterns of variation at linked neutral sites. For the most part, the authors provide intuitive explanations for the theoretical predictions and present a number of nice examples to illustrate these points. The end of the chapter primarily deals with theoretical models of epistatic selection. This section is quite technical with minimal connection to empirical data. Perhaps the most useful part of this latter section is the introduction of the quasi-linkage equilibrium approximation—a technique that is quite widely used amongst theoreticians today.

The final two chapters of the book focus on problems applying the core principles of earlier chapters. For example, Chapter 9 reviews models for the evolution of mating systems (e.g., selfing vs. outcrossing, dioecy vs. gynodioecy) emphasizing how genetic factors such as inbreeding depression and mode of inheritance affect the outcome of evolution. This chapter also provides an introduction to the problem of evolution of age-structured populations. While there are important issues that only arise in such populations (e.g., senescence), the authors emphasize that in most, but not all cases, population genetics theory based on discrete generations can be safely applied to populations with overlapping generations. The final chapter of the book covers topics in genome evolution, including codon bias and the evolution of recombination. I particularly enjoyed the section on the evolution of transposable element distributions. This was handled with a nice mix of theoretical predictions, intuitive explanations, and empirical data.

A strength and weakness of the book are the numerous models that are presented throughout its chapters. Many important models are presented and if a reader could understand them all (or even the majority of them), he or she would have gained an excellent working knowledge of population genetics theory. However, most of these models are presented in a concise form and this will make them challenging to follow for the typical evolution student with a limited theoretical background. For such students, I would highly recommend first reading the outstanding text by Otto and Day (2007) for an introduction to common techniques used in theoretical biology. In addition, or alternatively, the short book by Rice (2004) offers a guided tour through some of the basics of population genetics theory, even providing some helpful explanations of somewhat more advanced topics such as diffusion theory and the structured coalescent. Some familiarity with this type of material will allow the reader to get much more out of the Charlesworths’ text. It should be stated that most of the models are found in boxes and one could get through much of the text by focusing on the results while ignoring the details of how they were obtained. However, such an approach underutilizes a book that so clearly emphasizes the importance of theory.

It is worth noting that each chapter ends with a series of problems. A set of worked solutions is provided at the end of the book. These problems span a nice range of levels from simple application of the results to more sophisticated derivations and proofs. The solutions are quite helpful and provide more detail per step than shown elsewhere in the book. Working through these problems will lead students to a greater level of comfort with various modeling techniques as well as a more meaningful understanding of the important concepts.

In sum, Elements of Evolutionary Genetics is well-suited for serious readers who already have some familiarity with basic population genetics theory. The book covers a wide swath of material from classic population genetics through modern population genomics with the great expertise of authors who have made fundamental contributions across this spectrum. I imagine that this book will soon be found on bookshelves of evolutionary geneticists across the globe where it will serve as a useful reference for many years.

Book Review Editor: J. Thompson