A classic textbook example of adaptive radiation under natural selection is the evolution of 14 closely related species of Darwin's finches (Fringillidae, Passeriformes), whose primary diversity lies in the size and shape of their beaks^{1, 2, 3, 4, 5, 6}. Thus, ground finches have deep and wide beaks, cactus finches have long and pointed beaks (low depth and narrower width), and warbler finches have slender and pointed beaks, reflecting differences in their respective diets⁶. Previous work has shown that even small differences in any of the three major dimensions (depth, width and length) of the beak have major consequences for the overall fitness of the birds^{3, 4, 5, 6, 7}. Recently we used a candidate gene approach to explain one pathway involved in Darwin's finch beak morphogenesis⁸. However, this type of analysis is limited to molecules with a known association with craniofacial and/or skeletogenic development. Here we use a less constrained, complementary DNA microarray analysis of the transcripts expressed in the beak primordia to find previously unknown genes and pathways whose expression correlates with specific beak morphologies. We show that calmodulin (CaM), a molecule involved in mediating Ca²⁺ signalling, is expressed at higher levels in the long and pointed beaks of cactus finches than in more robust beak types of other species. We validated this observation with in situ hybridizations. When this upregulation of the CaM-dependent pathway is artificially replicated in the chick frontonasal prominence, it causes an elongation of the upper beak, recapitulating the beak morphology of the cactus finches. Our results indicate that local upregulation of the CaM-dependent pathway is likely to have been a component of the evolution of Darwin's finch species with elongated beak morphology and provide a mechanistic explanation for the independence of beak evolution along different axes. More generally, our results implicate the CaM-dependent pathway in the developmental regulation of craniofacial skeletal structures.

1. Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA
2. Decision Systems Group, Brigham and Women's Hospital, Harvard Medical School, 310 Thorn Building, 75 Francis Street, Boston, Massachusetts 02115, USA
3. Department of Oral Medicine, Infection and Immunity, Harvard School of Dental Medicine, 188 Longwood Avenue, Boston, Massachusetts 02115, USA
4. Institute of Molecular Pathology, Dr Bohr-Gasse 7, A-1030, Vienna, Austria
5. Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey 08544, USA
6. †Present address: Department of Developmental Biology, Harvard School of Dental Medicine, Boston, Massachusetts 02115, USA

Correspondence to: Clifford J. Tabin¹ Correspondents and requests for materials should be addressed to C.J.T. (Email: tabin@genetics.med.harvard.edu).The sequence of Darwin's finch CaM has been deposited at GenBank under accession number DQ386479, and the microarray data have been filed with ArrayExpress under the accession number E-MEXP-702.

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