Cited by 216Morphological variations and asymmetryDevelopmental Biology and Gene RegulationCraniofacial Disorders and Treatments

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Two developmental modules establish 3D beak-shape variation in Darwin's finches

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Mallarino, Ricardo, Grant, Peter R., Grant, B. Rosemary, Herrel, Anthony, Kuo, Winston P., Abzhanov, Arhat·2011·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.1011480108PMC PMC3053969

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Abstract

Bird beaks display tremendous variation in shape and size, which is closely associated with the exploitation of multiple ecological niches and likely played a key role in the diversification of thousands of avian species. Previous studies have demonstrated some of the molecular mechanisms that regulate morphogenesis of the prenasal cartilage, which forms the initial beak skeleton. However, much of the beak diversity in birds depends on variation in the premaxillary bone. It forms later in development and becomes the most prominent functional and structural component of the adult upper beak/jaw, yet its regulation is unknown. Here, we studied a group of Darwin's finch species with different beak shapes. We found that TGFβIIr, β-catenin, and Dickkopf-3, the top candidate genes from a cDNA microarray screen, are differentially expressed in the developing premaxillary bone of embryos of species with different beak shapes. Furthermore, our functional experiments demonstrate that these molecules form a regulatory network governing the morphology of the premaxillary bone, which differs from the network controlling the prenasal cartilage, but has the same species-specific domains of expression. These results offer potential mechanisms that may explain how the tightly coupled depth and width dimensions can evolve independently. The two-module program of development involving independent regulating molecules offers unique insights into how different developmental pathways may be modified and combined to induce multidimensional shifts in beak morphology. Similar modularity in development may characterize complex traits in other organisms to a greater extent than is currently appreciated.

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TGFβ signals through a heteromeric protein kinase receptor complex
Wrana, J. L., Attisano, L., Cárcamo, J. M., Zentella‐Dehesa, A., Doody, J. F., Laiho, M., Wang, X.-F., & Massagué, J. (1992) · Cell · doi:10.1016/0092-8674(92)90395-s · Cited by 1,528
Ecology and Evolution of Darwin's Finches
Snow, D. W., & Grant, P. R. (1988) · Journal of Animal Ecology · doi:10.2307/4785 · Cited by 1,166
Self-citation
The road to modularity
Wagner, G. P., Pavličev, M., & Cheverud, J. M. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2267 · Cited by 1,037
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Rodda, S. J., & McMahon, A. P. (2006) · Development · doi:10.1242/dev.02480 · Cited by 1,023
Function and biological roles of the Dickkopf family of Wnt modulators
Niehrs, C. (2006) · Oncogene · doi:10.1038/sj.onc.1210054 · Cited by 995
Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks
Shapiro, M. D., Marks, M. E., Peichel, C. L., Blackman, B. K., Nereng, K. S., Jónsson, B., Schluter, D., & Kingsley, D. M. (2004) · Nature · doi:10.1038/nature02415 · Cited by 861

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FB Gill Ornithology (Freeman, New York, 2007).
J Hanken, BK Hall The Skull (Univ of Chicago Press, Chicago, 1993).
DL Lack Darwin's Finches (Cambridge Univ Press, Cambridge, ([Eng.]). (1947).
RI Bowman Morphological Differentiation and Adaptation in the Galápagos Finches (Univ of California Press, Berkeley, 1961).

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Authors: Mallarino, R., Grant, P. R., Grant, B. R., Herrel, A., Kuo, W. P., & Abzhanov, A.
Affiliations: Harvard University (US)
Princeton University (US)
Muséum national d'Histoire naturelle (FR)
ORCID: Mallarino, Ricardo
Grant, Peter R.
Herrel, Anthony
Abzhanov, Arhat
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2011-02-22
Volume: 108
Issue: 10
Pages: 4057-4062
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.1011480108
PMC: PMC3053969
OpenAlex: W2070502859
Cited by: 216
References: 48
Citations by year: 2026: 7 · 2025: 11 · 2024: 13 · 2023: 7 · 2022: 9 · 2021: 19 · 2020: 9 · 2019: 14 · 2018: 9 · 2017: 13 · 2016: 33 · 2015: 14 · 2014: 21 · 2013: 17 · 2012: 12
FWCI: 23.45
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
HAL (submittedVersion)
Funders: National Science Foundation (0909695, 0616127)
Topics: Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Morphological variations and asymmetry
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Health Sciences › Medicine › Surgery › Craniofacial Disorders and Treatments
Keywords: Darwin's finches, beak shape, developmental modularity, β-catenin, Dickkopf-3, gene regulatory networks, avian evolution
MeSH terms: Animals, Beak, Biological Evolution, Humans, Species Specificity, DNA, Complementary, Receptors, Transforming Growth Factor beta, Oligonucleotide Array Sequence Analysis, Intercellular Signaling Peptides and Proteins, Finches, beta Catenin

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Two developmental modules establish 3D beak-shape variation in Darwin's finches

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