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 beaks. 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 diets. 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. Recently we used a candidate gene approach to explain one pathway involved in Darwin's finch beak morphogenesis. 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.

Speciation through evolution of sex-linked genes

“…An elegant combination of a candidate gene approach and microarray analysis has recently revealed molecules associated with different outcomes of embryonic development of the beak in Darwin's finches. A single factor, the bone morphogenetic protein 4 precursor (BMP4), appears to promote a deeper and wider beak (Abzhanov et al, 2004) whereas higher local expression of Ca 2 þ calmodulin-dependent protein kinase phosphatase (CaM) is associated with elongation of the beak (Abzhanov et al, 2006). Variation in beak shape along these different axes neatly matches different species of Darwin's Finches' ability to feed on seeds of different sizes (Bowman, 1961).…”

A multidisciplinary reconstruction of Palaeolithic nutrition that holds promise for the prevention and treatment of diseases of civilisation

“…It was recently shown that different levels of expression of a single gene might have resulted in the markedly different beak shapes and lengths of Darwin's finches. Experimental overexpression of the calmodulin gene in chicken embryos resulted in a significant increase in the length of their beaks (120,121) . These experiments suggest that small and seemingly insignificant changes can have profound implications for the evolution of anatomical size and shape and thereby provide great potential for explaining the origins of phenotypic variation (122) , including increases in brain and skull size.…”

Neural control of gene recruitment in metazoans

“…Studies on Darwin's finches have shown that the differences in the size and the shape of their beaks are related to the size of the regions where these neural crest cells recruit BMP4 (bone morphogenetic protein-4, which is responsible for the beak shape), BMP2 and BMP7 (for the size of the beak), as well as calmodulin (Abzhanov et al, 2006).…”