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Perspectives PERSPECTIVES overabundance of individuals within a species; OPINION differential survival of those most fit for the environmental circumstances; and the inheri- tance of those traits by the progeny of the sur- Opening Darwin’s black box: vivours. The molecular version of the modern synthesis showed that evolution can even teaching evolution through work over small timescales and therefore clearly showed how the principles of genetics developmental genetics and natural selection can, for example, explain the origins of pesticide-resistant insects and antibiotic-resistant bacteria2–4. Scott F. Gilbert The existence and efficacy of microevolu- tion is widely accepted, even by most cre- When biologists are asked to discuss the evolution. I discuss one possible way — there ationists5.But creationists are not concerned evidence for evolution at public forums, they are certainly others. about antibiotic-sensitive bacteria becoming usually use well-established microevolutionary Evolution has generated our planet’s biodi- antibiotic-resistant or about the beak shape examples. Although these examples show versity, and over the past century scientists changes of Galapagos finch species. They the efficacy of evolution within species, they have become able to explain the mechanisms have remained bacteria and finches, respec- often leave audiences susceptable to the by which changes in animal body structure can tively, so nothing much has changed — no arguments of creationists who deny that be produced, inherited and selected. Genetics new species has been created. To creationists, evolution can create new structures and is crucial to this understanding. The MODERN the synthesis of evolution and genetics can- species. Recent studies from evolutionary SYNTHESIS initially explained evolution through not explain how some fish became amphib- developmental biology are beginning to the mathematics of population genetics. ians, how some reptiles became mammals, or provide case studies that specifically address Although population genetics has remained how some apes became human (see the online these concerns. This perspective presents the core of the modern synthesis, it has also links box for a link to material dealing specifi- some of this new evidence and provides a come to include studies from ecology, biogeog- cally with arguments recently put forward framework in which to explain homology and raphy, paleontology, and more recently cytoge- by creationists). Behe6 named this inability phylogeny to such audiences. netics and molecular genetics. Population to explain the creation of new taxa through genetics, itself a marriage of Mendelian partic- genetics “Darwin’s black box”.When the box When asked to discuss evolution at public ulate inheritance and Darwin’s natural selec- is opened, he expects evidence of the Deity to forums, an hour or so is often given to outline tion, is able to explain how different alleles be found. However, inside Darwin’s black box the main principles of evolution and to give spread through the population, whereas cyto- resides merely another type of genetics — examples. I think that, until recently, our best genetics and molecular genetics are able to developmental genetics. examples came from microevolutionary stud- explain the origins of these alleles through If genetics is Darwin’s ‘missing evidence’7, ies — looking at evolution within a species. mutation and recombination. then developmental genetics is needed to However, although they are useful for Until recently, the best examples of evolu- complete the picture given by molecular and explaining evolutionary processes, focusing tion in action came from microevolutionary population genetics. Fifty years ago, British exclusively on microevolutionary studies left studies. Such studies explained, for instance, biologist C. H. Waddington was trying to openings for creationists to challenge whether how natural selection could cause moth col- bring developmental biology into the mod- species can be generated by evolutionary ouration to become darker and change the ern synthesis8–10, and he noted that evolution means. As well as providing new insights into beak shape in the Galapagos finches. For had two principal components. There was evolution, evolutionary developmental biol- the Galapagos finches, selection by drought the traditional component (that is, natural ogy has recently produced evidence that conditions allowed those individuals with cer- selection) that worked on adults that com- argues directly against the claims of creation- tain beak shapes to survive, transmit their pete for reproductive success, and an embry- ists, by shedding light on macroevolutionary beak shape to their offspring and change the ological component, in which variation (above the species-level) processes. Here, I beak morphology that had been characteristic was created and constrained.“The changes discuss some of this evidence and provide a of the species1.This illustrates the main tenets that produced new body plans…”, wrote framework for how we might wish to teach of natural selection: variation within a species; Waddington11,“…were inheritable changes NATURE REVIEWS | GENETICS VOLUME 4 | SEPTEMBER 2003 | 735 PERSPECTIVES in the patterns of embryonic development. Teaching phylogeny and homology But homology can be a tricky concept. If Changes in genotypes only have ostensible In 1859, Darwin wrote “It is generally acknowl- used alone (and some creationists imply that effects in evolution if they bring with them edged that all organic beings have been formed it is), it risks forming a circular argument alterations in the epigenetic processes by on two great laws — Unity of Type and wherein structures are considered homolo- which phenotypes come into being; and the Conditions of Existence” (REF.14).While natural gous because of common origin, and these kinds of change possible in the adult form of selection explained adaptation to the “offices of animals are said to have a common origin an animal are limited to the possible alter- existence”,embryonic homologies explained because they have homologous structures. An ations in the epigenetic system by which it is “unity of type” (REF.14).Together, they would independent assessment of ancestry and ori- produced.”Both the selective and the devel- produce the idea of ‘descent with modification’. gins is needed. Although we have this inde- opmental sides of evolution are important. In Using this concept, Darwin could explain the pendent assessment now, it was not avilable to 1977, the two sides of evolution began to be similarities of animal form through descent Darwin. Without this independent assess- bridged. Nobel Laureate François Jacob pro- from a common ancestor and the differences ment, the study of macroevolution became posed the idea that evolution was bricolage — by natural selection in different environments. embroiled in disputes about whether similar tinkering, not engineering12.Moreover,Jacob When introducing evolution to students, biol- structures were the result of common ances- claimed that evolutionary biologists should ogists usually concentrate on natural selection, try or convergence. The frustration about look at evolution not only in adults, but also the main mechanism of Darwinian evolution. whether similarities came from common during development, because evolution This is important. It shows that there is varia- ancestry (homology) or common environ- works not only on adults but also on the tion within a species; that most animals die ments (HOMOPLASY) caused biologists of the ‘recipes’ for adults. Therefore, to study large before reproducing; that the mortality can be first three decades of the twentieth century to changes in evolution, biologists needed to selective; and that the progeny resulting from leave this area of research and begin the micro- look for changes in the regulatory genes that such selection are more fit for their environ- evolutionary studies that related evolution to make the embryo, not just in the structural ment, having inherited the genes that made genetic variation within species (for example, genes that provide fitness within populations. their parents fit. But this is only half of the see REFS 16,17).“The geneticist…”,said William The last quarter of a century has borne out story. The other half concerns the unity of type Bateson in 1922, “…is the successor of the this idea. It took a while for developmental and the question of homology, that is, the fact morphologist.” (REF.18). genetics to reach maturity, but it can now be that animals are joined together into groups I find that I can teach the relationships of added to the mix of population genetics and with similar features. homologies and evolution best by looking at molecular genetics to explain evolution. one of the other passengers on the HMS Moreover, when developmental genetics is Beagle. The Tierra del Fuegan,York Minster, added, macroevolution can be explained was a bit older than Darwin, but like Darwin, much more easily. The microevolutionary “…I propose that students he had been trained in theology (FIG. 1a).York processes of mutation and recombination can will learn the principles of Minster had been abducted by Captain Fitzroy be analysed to determine how specific genetic on the first voyage of the HMS Beagle to the changes have created new types of organisms evolution most easily from southern tip of South America, and Fitzroy by altering their development. So, when con- examples of development.” had him educated
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