The DOI matches its Crossref record; 48 of the 48 references it cites were found in a registry or an index.
Two developmental modules establish 3D beak-shape variation in Darwin's finches
Open accessAbstract
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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“Taken together, these results support the fundamental prediction that macroevolutionary patterns are shaped by phenotypic modularity and integration, which are in turn determined by developmental processes (7, 11, 13, 16, 23).”
From Developmental origins of mosaic evolution in the avian cranium (2018) · cites this paper as [7]
Citations
Cites
Mechanisms of TGF-β Signaling from Cell Membrane to the Nucleus
Shi, Y., & Massagué, J. (2003) · Cell · doi:10.1016/s0092-8674(03)00432-x · Cited by 5,860
Nakashima, K., Zhou, X., Kunkel, G., Zhang, Z., Deng, J. M., Behringer, R. R., & de Crombrugghe, B. (2002) · Cell · doi:10.1016/s0092-8674(01)00622-5 · Cited by 3,608
Evo-Devo and an Expanding Evolutionary Synthesis: A Genetic Theory of Morphological Evolution
Carroll, S. B. (2008) · Cell · doi:10.1016/j.cell.2008.06.030 · Cited by 2,067
Aneurysm Syndromes Caused by Mutations in the TGF-β Receptor
Loeys, B., Schwarze, U., Holm, T. M., Callewaert, B. L., Thomas, G. H., Pannu, H., Backer, J. F. A. D., Oswald, G. L., Symoens, S., Manouvrier‐Hanu, S., et al. (2006) · New England Journal of Medicine · doi:10.1056/nejmoa055695 · Cited by 1,677
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-citationWagner, G. P., Pavličev, M., & Cheverud, J. M. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2267 · Cited by 1,037
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
Research works printed but not linked: 4
- 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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Sorted by citations
Evolution of Darwin’s finches and their beaks revealed by genome sequencing
Lamichhaney, S., Berglund, J., Almén, M. S., Maqbool, K., Grabherr, M. G., Barrio, Á. M., Promerová, M., Rubin, C., Wang, C., Zamani, N., et al. (2015) · Nature · doi:10.1038/nature14181 · Cited by 993
Self-citationThe problem of pattern and scale in ecology: what have we learned in 20 years?
Chave, J. (2013) · Ecology Letters · doi:10.1111/ele.12048 · Cited by 462
“Even more remarkable – and important for the point here – is the fact that the developmental basis for rapid changes in the shape of Darwin's finch beaks has been unravelled (Mallarino et al. 2011 ), offering a mechanistic basis for trait change observed in the wild.”
BackgroundDevelopmental Bias and Evolution: A Regulatory Network Perspective
Uller, T., Moczek, A. P., Watson, R. A. R., Brakefield, P. M., & Laland, K. N. (2018) · Genetics · doi:10.1534/genetics.118.300995 · Cited by 286
Developmental origins of mosaic evolution in the avian cranium
Felice, R. N., & Goswami, A. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1716437115 · Cited by 249
“Mosaic evolution has since become a central part of understanding avian origins and diversification (3–6), but it is rarely quantified (7).”
BackgroundThe shapes of bird beaks are highly controlled by nondietary factors
Bright, J. A., Marugán-Lobón, J., Cobb, S. N., & Rayfield, E. J. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1602683113 · Cited by 258
“The trend for the face to elongate with allometry has also been noted in mammals (17) and is postulated to be related to heterochrony, an important factor in the evolution of birds from dinosaurs (46) and a demonstrated mode of generating diversity of beak forms in Darwin’s finches (6, 9).”
Background
Metadata
- 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)
- 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
- 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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