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The calmodulin pathway and evolution of elongated beak morphology in Darwin's finches

Abstract

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 beaks1,2,3,4,5,6. 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 birds3,4,5,6,7. 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.

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Figure 1: Microarray analysis in different finch species.
Figure 2: Comparative analysis of CaM expression in finches.
Figure 3: Functional analysis of CaM-dependent pathway in beak development.
Figure 4: BMP- and CaM-dependent signalling regulates growth along different axes, facilitating the evolution of distinct beak morphologies in Darwin's finches.

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Acknowledgements

We thank all field assistants and participants of the field collecting trips—M. Protas, J. Chavez, G. Castaneda, O. Perez, F. Brown, A. Aitkhozhina, M. Gavilanes, M. Paez, K. Petren, J. Podos and S. Kleindorfer—for their advice with species identification and other advice; Charles Darwin Research Station on Santa Cruz Island and The Galápagos National Park for permits and logistical support; and M. Kirschner for discussions that led to the inception of this project. A.A. was supported by the Cancer Research Fund of a Damon Runyon–Walter Winchell Foundation Fellowship. This project was funded by a program project grant from the NIH to C.J.T. Author Contributions A.A. performed embryonic material collection, microarray probe preparation, microarray hybridizations and scanning, sectioning of material, in situ hybridizations and CaMKII functional analysis in chicken embryos. W.P.K. conducted all relevant bioinformatics analyses. C.H. constructed the RCAS virus carrying the constitutively active version of CaMKII. B.R.G. and P.R.G. provided logistics and secured permits for the fieldwork on the Galápagos Islands. C.J.T. conceived and supervised the project. A.A., B.R.G., P.R.G. and C.J.T. co-wrote the manuscript. All authors discussed the results and commented on the manuscript.

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Correspondence to Clifford J. Tabin.

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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. Reprints and permission information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

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Abzhanov, A., Kuo, W., Hartmann, C. et al. The calmodulin pathway and evolution of elongated beak morphology in Darwin's finches. Nature 442, 563–567 (2006). https://doi.org/10.1038/nature04843

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