FITNESS LANDSCAPES AND THE ORIGIN OF SPECIES1

Abstract

BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne's Terms of Use, available at www.bioone.org/page/terms_of_use. Recently, there has been an upsurge of interest in mech-anisms of speciation—reflected in a spate of conferences, prominent papers, and in reviews such as Howard and Ber-locher (1997) and in Trends in Ecology and Evolution 2001, volume 16, number 7. Of course, the origin of species has been a central issue throughout the history of evolutionary biology, but it was relatively neglected during the last de-cades of the 20th century as attention focused on the causes of molecular variation, on measuring natural selection in the wild, and on reconstructing phylogenies. Recent work on speciation is scattered over many disciplines. Empirical work has come from phylogenetics and biogeography, laboratory experiments, field studies of diverging populations, and the classical genetics of differences between (mostly) Drosophila species. Theoretical work has been similarly scattered, draw-ing on evolutionary ecology, population genetics, and, most recently, physics. Thus, the publication last year of two books that draw together this disparate field is timely and welcome. Coyne and Orr (2004) review the experimental and compar-ative evidence, while Gavrilets (2004) summarizes the var-ious theories. Treatment at book length is especially neces-sary in this area, because many different lines of argument need to be synthesized in a coherent way. Gavrilets' book is divided into three sections: fitness land-scapes, the Bateson-Dobzhansky-Muller (BDM) model, and the joint action of disruptive selection and nonrandom mat-ing. The first section establishes the general properties of fitness landscapes and argues for the inevitability of nearly neutral networks—sets of genotypes that are mutationally accessible and that have similar and high fitness. The second section reviews a model of speciation introduced by Bateson in 1909, but usually associated with Dobzhansky and Muller. Here, reproductive isolation evolves as a side effect of di-vergence across nearly neutral networks; crucially, isolation need not be expressed during divergence. The final section reviews models of sympatric speciation, in which disruptive selection drives the evolution of assortative mating. In such models, speciation is an adaptation that prevents interbreed-ing between distinct, well-adapted genotypes. How useful are ''fitness landscapes'' for understanding the origin of species? The idea was introduced by Sewall Wright in 1931, primarily as a metaphor for understanding how pop-ulations can adapt when gene interactions cause multiple fit-ness peaks—hence, Wright's original term, adaptive land-scape. This way of understanding evolution has been criti-cized for several reasons (Provine 1986). First, Wright in-troduced two quite different versions of his adaptive 1 Fitness Landscapes and the Origin of Species. Sergey Gavrilets. 2004. Princeton University Press, Princeton, New Jersey. 476 pp. HB $99.50, ISBN 0-691-11758-6; PB $39.50, ISBN 0-691-11983-X.