Tinkering : the microevolution of development

Recent developments in evolutionary biology have confl icting implications for our understanding of the developmental bases of microevolutionary processes. On the one hand, Darwinian theory predicts that evolution occurs mostly gradually and incrementally through selection on small-scale, heritable changes in phenotype within populations. On the other hand, many discoveries in evolutionary developmental biology—quite a few based on comparisons of distantly related model organisms—suggest that relatively simple transformations of developmental pathways can lead to dramatic, rapid change in phenotype. Here I review the history of and bases for gradualist versus punctuationalist views from a developmental perspective, and propose a framework with which to reconcile them. Notably, while tinkering with developmental pathways can underlie large-scale transformations in body plan, the phenotypic effect of these changes is often modulated by the complexity of the genetic and epigenetic contexts in which they develop. Thus the phenotypic effects of mutations of potentially large effect can manifest themselves rapidly, but they are more likely to emerge more incrementally over evolutionary time via transitional forms as natural selection within populations acts on their expression. To test these hypotheses, and to better understand how developmental shifts underlie microevolutionary change, future research needs to be directed at understanding how complex developmental networks, both genetic and epigenetic, structure the phenotypic effects of particular mutations within populations of organisms. 2007 Tinkering: the microevolution of development. Wiley, Chichester (Novartis Foundation Symposium 284) p 1–19 ‘Tell you what though, for free, terriers make lovely fi sh. I mean I could do that for you straight away. Legs off, fi ns on, stick a little pipe through the back of its neck so it can breathe, bit of gold paint, make good . ’ Pet Conversion Sketch, Monty Python’s Flying Circus, Episode 10 In a favourite Monty Python sketch, an unscrupulous and imaginative pet salesman describes a few simple transformations by which he can convert a dog into a fi sh. The sketch is preposterous for many reasons, not the least of which 2 LIEBERMAN & HALL is the feigned biological naïveté of the customer. The pet store’s unconventional practices also ridicule scenarios by which non-evolutionary processes might generate novel, adaptive forms. It has traditionally been believed that evolution occurs gradually within populations from the accrual of many incremental, tinkering-like transformations of existing structures. The radical transformation of a terrier into a fi sh is not only an evolutionary reversal but also absurdly un-Darwinian: ‘As natural selection acts solely by accumulating slight, successive, favourable variations, it can produce no great or sudden modifi cation; it can only act by short and slow steps (Darwin 1859, p 471). ’ Darwin, of course, didn’t know the mechanisms by which evolutionary change occurs, but he clearly believed in gradualism (Mayr 1991). The heart of his theory is that each generation within an interbreeding population inherits a range of phenotypic variations. Because of relentless competition caused by geometric rates of reproduction, limited resources, and/or environmental change, those variations that confer some benefi t to an organism’s chances of surviving and reproducing will increase in frequency. The accumulation of such variations over time leads not only to organisms that are better adapted to their environments, but is also assumed to be implicated in speciation—the most important type of evolutionary change. Darwin and his contemporaries were working before modern genetics was born, and they struggled with problems of missing information and temporal scale. Interestingly, many of us continue to struggle with the same challenges even though we now have a much better grasp of the fundamentals of genetics. It requires little imagination to see how selection or other processes such as drift and founder effects can lead to different varieties of fi nches or tortoises; but it is considerably harder to understand how the same processes can lead from common ancestors to forms as diverse as whales and hippos, or even humans and chimpanzees. A part of this problem of comprehension lies in the nature of the fossil record, whose inadequacies lead inevitably to gaps. Most intermediate forms no longer exist, and (a bit) like Bishop Berkeley’s conundrum of the falling tree, how can we understand a given transformation if we can’t observe it? We are thus hampered by missing evidence and by a limited understanding of the mechanisms by which one form can transform into another. How does a jaw become an ear, a scale become a tooth, or a swim bladder become a lung? As we begin to understand more about the developmental processes that generate transformations leading to intermediate forms, we can begin to see a more complete and satisfying picture of what really happened in evolution and why. The burgeoning fi eld of evolutionary developmental biology (EDB) has had a major impact on our thinking about evolution above the level of the species (macroevolution). EDB has become a vital and exciting fi eld by reopening the black box—so long ignored by evolutionary biologists—of the developmental bases for INTRODUCTION 3 evolutionary change (see Hall 2003). At the same time, EDB has helped invigorate research on evolution within developmental biology. A key element in the origins of EDB was a set of discoveries in developmental genetics in a few model systems and their extension to non-model system organisms. About 20 years ago we remember the excitement of the fi rst papers on homeobox gene regulation that started to fi ll the pages of Nature and Science (e.g. McGinnis et al 1984, Shepherd et al 1984, Dolle et al 1989, Kessel & Gruss 1990, Hunt et al 1991). Other key infl uences were Gould (1977), Raff & Kaufman (1983) and Atchley & Hall (1991), all of which were eye openers for palaeontologists and other biologists because they outlined more integrative approaches to addressing the evolutionary questions we wanted to study. Suddenly, it seemed possible for palaeontologists, long preoccupied with major trends in macroevolution above the level of the species, to test hypotheses about how evolutionary change occurred within populations (microevolution) and during speciation events. EDB has thus had widespread effects, even in fi elds remote from developmental biology. For example, in the fi eld of human evolution, researchers have begun to rethink issues of homology, and to ask questions about the developmental bases for the transformations we observe in the fossil record (e.g. Lieberman 1999, Lovejoy et al 1999, Lieberman et al 2004, Pilbeam 2004, Hlusko 2004). Not surprisingly, EDB itself is evolving rapidly. Many of EDB’s most spectacular and early advances focused on large-scale shifts in body plan. A typical research framework has been to compare the developmental mechanisms that underlie differences in development between two or more standard model organisms (chickens, mice, zebrafi sh, fruit fl ies and nematodes) in their phylogenetic context. These comparisons have led to many basic insights about the genetic and developmental bases for major variations in animal body form. However, more and more organisms are now being studied in greater and greater detail and in taxa with closer and closer relationships. One useful consequence of this combination of increased breadth and depth is to permit comparisons of large-scale evolutionary shifts with smaller-scale differences between closely related species. Given that natural selection occurs most fundamentally on individuals within populations, it is especially appropriate that researchers are increasingly studying the developmental bases for the generation of variation within populations (e.g. Stern 2000, Brakefi eld 2003, Shapiro et al 2004, Frankino et al 2005). As EDB increasingly turns its focus to microevolution and the developmental bases of within-species variation, we can look forward to a new synthesis of genomics, EDB and population genetics. Ironically, one issue persistently raised by the growing focus on microevolution within EDB and other fi elds is equivalent to the problem of scale, noted above, that confronted Darwin and his contemporaries: are the evolutionary developmental bases of phenotypic change at the microevolutionary and macroevolutionary