Evolution, the Extended Synthesis

5 - Integrating Genomics into Evolutionary Theory

5 Integrating Genomics into Evolutionary Theory Gregory A. Wray Many of the major advances in evolutionary biology have grown out of synthesis between disparate disciplines. Indeed, synthesis was present right from the beginning. Darwin was a consummate integrator of information :in formulating his theory of natural selection he drew key insights not only from the scientific literature and his own extensive observations of natural history, but also from geology and sociology. He also drew on medicine, plant and animal breeding, and the nascent fields of embryology and paleontology to provide material evidence in support of his ideas. Many decades later, the Modern Synthesis integrated fundamental advances from Mendelian and quantitative genetics into evolutionary thinking, while a more contemporary view of paleontology played a smaller but significant part of the integration. The Modern Synthesis is often considered the most pivotal era in the history of post-Darwinian thinking about evolution. Witness the title and topic of the present volume: the Modern Synthesis is the benchmark against which all other advances in evolutionary theory are measured (Pigliucci 2007). A compelling case could be made, however, that information about the material basis for heredity has been just as transformative to evolutionary biology as the Modern Synthesis. Understanding the structure of DNA, the physical nature and variety of mutations, the molecular consequences of different kinds of mutations, and the mechanisms by which genes produce traits have all led to profound insights into evolutionary processes and mechanisms (Lynch 2007).Although the impact of molecular biology on evolutionary thinking was spread over several decades rather than concentrated into just a few years, the insights that have emerged from it are as profound as any that emerged from the Modern Synthesis. A prominent example is Kimura’s Neutral Theory, which was motivated by empirical observations of genetic variation. The development of the Neutral Theory was not a natural extension of the Modern 98 Gregory A. Wray Synthesis, and could not have happened in a premolecular era. Yet Kimura’s ideas have utterly transformed how evolutionary biologists model and analyze evolutionary processes at a genetic level. A century and a half after the publication of the Origin of Species, evolutionary biology is once again in a period of extraordinary integration and synthesis (Feder and Mitchell-Olds 2003; Rose and Oakley 2007; Pagel and Pomiankowski 2007). A quick perusal of the chapters in this book reveals that the impetus for this excitement is coming from several sources. Unquestionably, however, one of the most important of these is the availability of genome-scale data sets from many species and from many individuals within some species. As methods for gathering genomic data become more robust and as prices for doing so drop, consideration of these very large and rich data sets will become routine in every facet of evolutionary biology. The impact will be profound. In this chapter, I discuss some of the opportunities and challenges that the genomic era brings to evolutionary biology, and some of the ways current research into genome evolution is extending the Modern Synthesis. Extending the Modern Synthesis to the Genome Although genomics is one of the youngest branches of biology, two distinct phases in its history are already over.The first is the era when information was limited to genome sequences from just a handful of widely divergent species. The number of genome sequences is rising exponentially : prokaryotic genomes are being sequenced on a daily basis, and eukaryotic genome sequences appear almost weekly. Alignments of entire mammalian genomes and reconstructed ancestral genome sequences for internal nodes (Ma et al.2006;Blanchette et al.2004) signal the beginning of a new era in understanding how genomes evolve. Sequenced genomes from closely related species provide particularly appealing subjects for evolutionary analyses, and this information is now available for several clades (e.g., Kellis et al. 2003; Stark et al. 2007; Rhesus Macaque Genome Sequencing and Analysis Consortium 2007). It is possible to apply comparative methods in a serious way to sequences at the scale of tens of kb up to entire genomes (e.g., A. G. Clark et al. 2003; Doniger and Fay 2007; Hahn 2007), based on information that is accessible through the Web. As ultrahigh throughput sequencing technologies become more robust and affordable, it is becoming possible to generate whole-genome sequences and very large population samples of targeted regions at costs that a single lab group can contemplate. Integrating Genomics...