Nature Journal Club

Judith E. Mank

Edward Grey Institute, Department of Zoology, University of Oxford, UK

An evolutionary biologist compares genomic complexity to modern art.

Like many students of evolutionary biology, I was taught that genes encode physical traits, or ‘phenotypes’, that are the focus of natural selection — a model with clear, direct links and few, if any, complications. Over the past few years, I have found it increasingly difficult to reconcile this simple model connecting genes and the organisms they encode with the burgeoning data of systems biology, which show the genome as a heaving tangle of interconnections. Given the complexity of the genome, how can selection target any single gene without unintended consequences?

Trudy Mackay at North Carolina State University in Raleigh and her collaborators have begun to resolve the opposing genomic and evolutionary world views by examining the systems genetics that underlie phenotypes in the fruitfly Drosophila melanogaster (J. F. Ayroles et al. Nature Genet. 41, 299–307; 2009). They do this by comparing data on the abundance of more than 10,000 DNA transcripts with whole-organism traits, such as fitness and lifespan, in 40 fruitfly lines.

The researchers show that aggregates of genes correlate with distinct characteristics in flies, and that these modules are connected, with groups of genes associated with multiple phenotypic traits. This elegant complexity is best conveyed by the figures in the paper, some of which look as though they were lifted off the walls of a modern-art gallery.

The group’s work provides a post-genomic framework for dissecting the intricate underpinnings of organismal biology. More importantly, the paper demonstrates that key topics in traditional evolutionary studies, such as heritability, and more recent concepts, such as pleiotropy (whereby one gene affects multiple traits), are related. As such, they must be considered together to build a complete understanding of how selection acts through the phenotype to sculpt the genome.

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