Functional evo-devo Casper J. Breuker 1, 2 , Vincent Debat 1, 3 and Christian Peter Klingenberg 1 1 Faculty of Life Sciences, University of Manchester, Michael Smith Building, Oxford Road, Manchester, UK, M13 9PT 2 Department of Biology, Group of Evolutionary Biology, University of Antwerp, Groenenborgerlaan 171, B-2020 Antwerp, Belgium 3 Museum National d’Histoire Naturelle, De ´ partment Syste ´ matique et Evolution, Laboratoire d’Entomologie, 45 rue Buffon, 75005 Paris, France Functional factors such as optimal design and adaptive value have been the central concern of evolutionary biology since the advent of the New Synthesis. By con- trast, evolutionary developmental biology (evo-devo) has concentrated primarily on structural factors such as the ways in which body parts can be built. These different emphases have stood in the way of an inte- grated understanding of the role of development in evolution. Here, we try to bridge this gap by outlining the relevance of functional factors in evo-devo. We use modularity and the view of development as a flexible evolutionary system to outline a unified perspective that includes both structural and functional aspects. Development as a factor in evolution Whereas development has long been recognized as being important in evolution, its role as an evolutionary factor has only begun to be investigated relatively recently with the study of heterochrony [1] and developmental quanti- tative genetics [2]. The rise of evolutionary developmental biology (evo-devo) as a biological discipline has brought about several changes in perspective [3,4]. In addition to a new focus on the developmental mechanisms that generate new variation, the discovery of the widespread evolution- ary conservation of genes with prominent roles in devel- opment (e.g. Hox genes [5]) has revived an interest in comparative studies at a large phylogenetic scale. This shift of interest and emphasis has drawn attention away from the traditional focus of evolutionary studies, namely the adaptive value and functional significance of phenotypic traits. Here, we attempt to integrate functional considerations with the central concepts emerging from evo-devo. We hope that this will contribute to a more unified understanding of the role of development in adap- tive evolution. Structural and functional factors in evolution The debate about the relative importance of intrinsic structural factors and external adaptation in biological evolution has a long history [6,7]. By the mid-20th century, the neo-darwinian New Synthesis had established adapta- tion as the central theme of evolutionary biology, such that the primary research emphasis was on the external factors that shaped organisms through natural selection. The discovery of ample genetic variation in natural populations suggested that the raw material for natural selection is plentiful. It was therefore expected that selection would produce optimal solutions in an engineering sense [8], where each organ is optimised for performing certain functions that confer maximum fitness jointly to the organ- ism. The evolution of a trait could therefore be explained by its function. Neo-darwinian theory has emphasized function at the expense of structural and historical concerns. When cla- distics, the study of relationships among organisms through the branching of evolutionary lineages, became the dominant direction of systematics in the 1980s, histor- ical considerations entered mainstream evolutionary biol- ogy under the headings of phylogenetics and the comparative method [9]. The discovery of the pervasive conservation of Hox genes [5] and their expression patterns across animal phyla was surprising because it was at odds with the expectation that genetic and developmental systems would evolve just as much as the morphological traits they gen- erate [7]. This discovery of conserved developmental genes, along with similar findings for other families of genes involved in key developmental processes, provided an important impetus for the emergence of evo-devo as a discipline. Evo-devo also awakened a renewed interest in phylotypic stages [4], developmental stages shared by the species across entire phyla in spite of vast differences in the development and morphology before and after that stage, and coined the new concept of the zootype [10],a hypothetical ground plan for all bilaterian animals. These ideas were tied explicitly to the concept of the archetype, the idea of a common body plan that underlies the varia- tion in a group (such as the vertebrates) that had been rejected vehemently by the main exponents of the New Synthesis [7]. Altogether, these discoveries have attracted new attention to structural factors. Evo-devo has also revived structuralist arguments that emphasized the importance of generic physical factors [11,12], such as the forces driving morphogenetic move- ments, in the development and evolution of organismal forms. The combination of such factors with findings from developmental genetics has made it possible to formulate general models of pattern formation [13]. Models of this kind have been applied to the variation and morphological innovation in the patterns of mammalian tooth cusps [14] and have subsequently been confirmed experimentally [15]. Given its primary focus on large-scale phylogenetic comparison and developmental mechanisms generating variation, evo-devo has emphasized a structural and partly historical perspective on evolution, but has not concerned Opinion TRENDS in Ecology and Evolution Vol.21 No.9 Corresponding author: Klingenberg, C.P. (cpk@manchester.ac.uk). Available online 30 June 2006 www.sciencedirect.com 0169-5347/$ – see front matter ß 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2006.06.003