All You Ever Wanted to Know about Microevolution

Evolutionary Genetics: From Molecules to Morphology By Singh Rama S., Krimbas Costas B. Cambridge: Cambridge University Press (2000). 720 pp. $95.00It is probably fair to say that, in the second half of the twentieth century, no single person has had a greater influence on the progress of evolutionary biology than Richard C. Lewontin. Perhaps testifying to the still tender age of this field, Lewontin has made key contributions to both theory and experiment. As a theorist, he initiated, with M. Kimura and K.-i. Kojima, the formal analysis of natural selection acting on more than one locus. As an experimentalist, he, J. L. Hubby, and H. Harris used protein electrophoresis to discover that natural populations harbor a remarkable amount of genetic variability (polymorphism). This fundamental fact, now taken for granted, was an astonishing revelation 35 years ago. Also, Lewontin, himself a student of Theodosius Dobzhansky, was the mentor of Martin Kreitman when the latter, in 1983, carried the Chetverikov-Dobzhansky program of comprehensive investigation of genetic variability down to the genome sequence level, by discovering what is now known as single nucleotide polymorphisms (SNPs) in Drosophila melanogaster.Thus, one can expect much from a collection of essay produced by students and colleagues of Lewontin to celebrate his 65th birthday. Indeed, the 32 articles that constitute this volume cover just about everything within the field of microevolution and, at least in this sense, the volume lives up to the high expectations. It can be recommended both to professional microevolutionists and to biologists who know little about microevolution, but want a serious introduction to this field.The opening essay, by Lewontin himself, introduces the basic concepts of microevolution, genotype space and phenotype space, as well as the main subject of this field of biology, intrapopulation genetic variability and the factors affecting its dynamics (mutation, natural selection, random genetic drift, etc.). Several articles, in particular one by Schaeffer and Aguade, deal with genetic variability at the molecular level and with attempts to deduce the properties of natural selection from the patterns of this variability. Perhaps surprisingly, it turns out that the most conspicuous form of selection at the DNA level is purifying (stabilizing) selection that favors alleles that are already common. Detecting purifying selection does not require much special effort because its effect can be seen in any comparison of homologous DNA sequences from sufficiently different species—those sequence regions that are conserved are assumed to be under purifying selection. In contrast, detecting directional selection (which constantly favors initially rare alleles and can eventually cause their fixation) and balancing selection (which favors rare alleles only as long as they remain rare) turned out to be unexpectedly difficult. There are several convincing studies on both these forms of selection, but in general, the progress in their understanding remains slow. As a result, we possess considerable knowledge of the sequences that are responsible for the similarity between different species (e.g., humans and mice), but we understand very little about the genomic basis of the interspecies differences.Another key problem of microevolution, the connection between variability of genotypes and that of phenotypes is considered in four articles. In particular, Charlesworth and Huges review the current knowledge of the forces that maintain variability of life-history traits. Because such traits are certainly selectively important, the key Darwinian principle (formalized in Fisher's Fundamental Theorem of Natural Selection) seems to dictate that only the fittest survive and any genetic variability is abolished. The data show, however, that life-history traits are highly genetically variable. Charlesworth and Hughes conclude that deleterious mutations play a major role in maintaining this variability, but other factors also must be involved.Several articles, including those by Franklin and Feldman, by Slatkin, and by Uyenoyama, deal with hard core population genetics theory, including multilocus selection, evolution of recombination and breeding systems, coalescence of allele genealogies, and population structure. Equations are inevitable in any discussion of these subjects, but the articles are generally accessible and will be useful as introductory reading. In particular, Slatkin provides a neat overview of the coalescence framework, which during the last two decades plays an increasingly important role (alongside with diffusion equations) in the theory of genetic drift.Different aspects of speciation are also considered. Specifically, Coyne and Orr present a useful survey of a large body of data on postzygotic isolation. Crosses between closely related species often produce hybrids that are partially inviable and/or sterile. Genetic analysis of such hybrids led to discovery of incompatible genes, accumulated in the course of independent evolution of different species, whose simultaneous presence within hybrids leads to troubles. One can anticipate that in the next decade many cases of reproductive isolation between species will be traced all the way down to the failure of some protein–protein or DNA–protein interactions. However, a notable omission in this section is the lack of an adequate discussion of the theory and data on sympatric speciation, that is the splitting of one geographically unstructured population into two species.Finally, four essay attempt to define the role of microevolution in the overall picture of the evolutionary process. The topics include evolution of form and function at different levels, evolution of behavior, ecological interactions, and others. These essay, particularly those by Felsenstein and Maynard Smith, are insightful and certainly a pleasure to read, but the picture emerging from them, and in fact, from the entire book is far from idyllic.During most of the twentieth century, evolutionary biology was shaped by what may be called Chetverikov–Dobzhansky paradigm: it was assumed, sometimes implicitly, that understanding the dynamics of genetic variability within populations is the key to understanding all evolution. Every time a new method made it possible to study genetic variability at a new level (chromosomal inversions in 1937, protein electrophoresis in 1966, DNA sequencing in 1983), new, deep insights into the very nature of evolution have appeared imminent. Indeed, significant progress has been made, but the astonishing growth of data (just imagine Hermann Muller or Alfred Sturtevant searching a database of human SNPs, or for that matter, the complete sequence of the Drosophila melanogaster genome) somehow has not been matched by a commensurate growth in understanding. Sometimes it is hard to avoid the nagging feeling that we have reached a point of diminishing return when investigation of increasingly elaborate models and rapidly growing databases of microevolutionary data leads only to limited progress. How much remains to be learned from studying the dynamics of genetic variability? In other words, is the Chetverikov–Dobzhansky paradigm still alive and well?This book does not provide a conclusive answer. The majority of the authors apparently believe that the traditional approach will yield much more. In contrast, Felsenstein leans toward the opinion that a new paradigm is needed. We believe that both views have merit. Certainly, the classical microevolutionary methodology is not yet exhausted. For example, the genomic rate of deleterious mutations, a key parameter of several theories, has never been measured with sufficient accuracy for any multicellular species. However, no amount of analysis of genetic variation is going to give us an understanding of how, say, eukaryotic chromatin or the vertebrate eye have evolved from much simpler structures. With multiple, complete genome sequences now available for comparison, new approaches should allow us to attack these truly fundamental evolutionary issues. In this context, it is somewhat disappointing that this book does not address issues such as the evolution of genome organization, of three-dimensional structure of proteins, and of metabolic and signal transduction pathways. It seems likely that these subjects will dominate the study of evolution in the coming century.However, this is probably asking for too much too soon. The Chetverikov–Dobzhansky paradigm has been and still is extremely successful and certainly will be a part of the foundation of new evolutionary biology, whatever shape it takes. Evolutionary Genetics does justice to this paradigm and should be recommended to anyone who wants to understand it.