Evolutionary Quantitative Genetics

Reviewed by Paul David Polly

Article number: 1.2.2R
1 August 1998

by Derek A. Roff, 1997
Chapman and Hall
London & New York.  xii+ 493 pages. 
ISBN/ISSN: 0-412-12971-X, US $49.95; UK £39.00; Canada $75.95 (paperback). 

The field of quantitative genetics seldom enters the minds of most paleontologists. Thanks to generations of introductory biology texts, quantitative genetics is often equated with dirty moths waltzing the Hardy-Weinberg during the Industrial Revolution. And according to a few paleobiological pundits, quantitative genetics herself is dancing a dogmatic Red Queen's Shuffle to a slow neo-Darwinian blues. Eldredge (1995) began Reinventing Darwin by arranging a dichotomous dinner table at which geneticists (he apparently meant population or quantitative geneticists) and paleontologists sat glaringly across from one another with "diametrically opposed suppositions of how evolutionary biology should be conducted" (p. 2). When Eldredge looked at his "genetically imbued colleagues" he saw "slavish adherence to a tradition that dates back to Darwin, serving as the pivotal article of faith in a geneticist's approach to understanding evolution" (p. 3). As Eldredge told the story, quantitative genetics is about generation-by-generation changes in genetic information within a population. Moreover, Eldredge accused geneticists of extrapolating their patterns through the vastness of geologic time and triumphantly announcing "QED". He seems to firmly believe that geneticists haughtily dismiss paleontology as having no information about genetic change nor, therefore, about evolution. 

As with almost all caricatures, Eldredge's portrait was mostly a self-serving chalk-outline into which he hoped to position a body. Much of the focus of quantitative genetics is on morphologic - not just genetic - evolution and there are few practitioners who would consider the topic of tempo and mode in evolution (especially long-term evolution) exhausted. The story of quantitative genetics as narrated by Provine (1971) was a tale of synthesis of Darwinism, Mendelism, and biometry at the turn of the 20^th Century. It was the resolution and dénouement of the decades-long conflict between the saltationist Mendelians (mostly geneticists) and the gradualist Darwinians (mostly morphologists and naturalists). The works of R. A. Fisher, J. B. S. Haldane, Sewell Wright, William Castle, and Sergei Chetverikov fused the concepts of morphologic and genetic variation, demonstrating for the first time that discontinuous genetic evolution could be reconciled with continuous morphologic change. Eldredge's reinvention has reversed the original roles of the adversaries, pitting punctuationist morphologists against gradualist geneticists. But his characterization is largely beside the point: Quantitative genetics is a diverse body of theory that attempts to predict the relationship of morphologic evolution (both variation and change over time) and underlying population genetic parameters. This also entails predicting the relationship between morphologic evolution and non-genetic parameters such as maternal effects, developmental constraints, population size, geographic distributions, inbreeding, neutral evolution, population bottlenecks, selective factors, and others. Usually theoretical models in quantitative genetics are constructed with the assumption that they will be tested. This is most commonly done using computer modeling, field data, or laboratory experiments; however, quantitative genetics predictions are not usually tested with long-term paleontologic data. This is partly because of the inherent difficulties in designing such tests, but even more because quantitative geneticists seldom stray into the paleontologic literature and paleontologists rarely read quantitative genetics papers. 

Those who crave such intellectual cross-fertilization will be interested in Derek Roff's new book, Evolutionary Quantitative Genetics. In it he sets out his view of the current state of the field, its major controversies, and its future. Heritability, correlation, selection, phenotypic plasticity, sex-related effects, small population size, and the maintenance of variation are all covered. Roff's intention is not to replace introductory texts such as Falconer and Mackay (1995), but to provide a critical review. He summarizes major contributions, evaluating the extent to which they have complemented or contradicted one another. Since evolution is his main concern, Roff emphasizes data and methods from field studies over lab experiments (which undoubtedly makes the book more interesting to those outside the field than it would be otherwise). In many cases, Roff tries to convince us of what he considers the best methods and the strongest conclusions, sometimes recommending continued work on certain areas. 

Heritability, the degree to which offspring inherit their physical traits from their parents, is a major theme of the book and the subject of its first chapter. This is a topic important not just within quantitative genetics, but in all evolutionary disciplines: One of the basic axioms of phylogenetic reconstruction, for example, is that shared traits are inherited from a common ancestor. Readers who are completely new to quantitative genetics may be surprised to find that the heritability of a trait is not all or nothing: Some traits are more heritable than others and virtually none are 100% or 0% heritable. Furthermore, the heritability of a trait changes over time, usually decreasing as a result of intense selection. This counter-intuitive behavior is because heritability (h²) is an estimated parameter. Roff discusses several variants of the definition and estimation of heritability, pointing out their relative effects on evolutionary models. He even questions the usefulness of heritability as a concept, but finds no better alternatives. The potential for heritability - as well as other factors like genetic correlation - to change in response to selection is a major theme throughout the rest of the book. 

Readers may also be surprised (especially given Eldredge's characterization of quantitative genetics) to hear Roff say that "as yet, there is no satisfactory theory to quantitatively predict the course of long-term selection" (p. 164). Response to selection is a product of heritability and selection differential; the difference in the frequency of a trait before and after selection. Because selection can modify both parameters, the response may also change over time; selection may neither be able to fix nor eliminate traits from a population. Furthermore, selection in one direction may be more effective than selection in the opposite for a given trait. Roff points out that there have been only four studies that applied quantitative genetics models of the effects of selection to natural populations and calls for more. Surprisingly, a graph presented in the chapter on directional selection shows the distribution of selection intensities in natural populations estimated from fossil populations! The paleontologic data cited come from Endler (1986), but Roff does not discuss them in his text. Paleontologists interested in quantitative genetics models will want to track down Endler's book and follow up the references in it (mostly to papers by Van Valen and Kürten). 

Evolutionary Quantitative Genetics is somewhat disappointing because it is not particularly effective at reaching new audiences. Roff limits his readership by not combining his exposition with a familiar problem. You will not find a novel reinterpretation of pre-Cambrian diversification, nor new insights into mass extinctions, nor a fresh perspective on the evolution of human cognition in this book. Nor does Roff integrate his material with that of related evolutionary disciplines, missing an opportunity to better Rudy Raff's wide-ranging synthesis of developmental biology, genetics, paleontology, and phylogeny in The Shape of Life (Raff, 1996). Most readers will even wonder whether Roff understands the significance of phylogeny for his work. In discussing reaction norms he states, "the ubiquity of their occurrence and the obvious advantages of such responses argues very strongly that selection has molded many, if not most, of them" (p. 199). Has Roff considered that reaction norms may have evolved only once? And his style is abrupt. Chapters often begin with a laconic introduction followed immediately by mathematical equations, in spite of Roff's claim that he wants to avoid burdening the reader with lengthy derivations. In many places the logic (at least to readers with limited quantitative experience) is obscured by reliance on a series of formulae to make a point. The most readable part of the book is the concluding summary. 

In spite of its shortcomings, Evolutionary Quantitative Genetics remains an authoritative overview of the field that will be of use to most students of morphologic evolution. In contradistinction to "The Geneticist" in Eldredge's "High Table" farce, Roff presents us with an intriguing and humble admission that the assumptions used heretofore in quantitative genetics have not been complex or powerful enough to predict long-term evolution in the lab, much less in natural populations. The majority of physical traits are influenced by neither a very few nor an infinite number of loci (which is the assumption of most theoretical models). Roff says that a better understanding of the actual genetic underpinnings of real characters will improve the ability of quantitative geneticists to model evolution in natural populations. Because experiments on selection based on multiple traits have not been successful Roff calls for an increased awareness of the roles of non-genetic factors - "morphology, physiology, and behavior" - in the correlation of traits. Phenotypic plasticity, population size (especially bottlenecks), and maternal effects are known to be important and common in evolution. Though theoretical treatments of these topics are just beginning, Evolutionary Quantitative Genetics provides the best critical review currently available. Roff ends with a plea for more tests of quantitative genetics predictions using natural populations: Paleontologists might consider how such tests could be made using fossil data.

References Cited

Eldredge, N. 1995. Reinventing Darwin: The Great Debate at the High Table of Evolutionary Theory. John Wiley & Sons, New York. 

Endler, J. A. 1986. Natural Selection in the Wild. Princeton University Press, Princeton. 

Falconer, D. S. and T. F. C. Mackay. 1995. Introduction to Quantitative Genetics. 4^th Edition. Addison Wesley Longman, New York. 

Provine, W. B. 1971. The Origins of Theoretical Population Genetics. Chicago University Press, Chicago. 

Raff, R. A. 1996. The Shape of Life: Genes, Development, and the Evolution of Animal Form. Chicago University Press, Chicago.