Two developmental modules establish 3D beak-shape variation in Darwin's finches
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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, the results support the fundamental prediction that macroevolutionary patterns are shaped by phenotypic modularity and integration, which are in turn determined by developmental processes.
“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]
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Jablonski, D. (2022) · Evolutionary Biology · doi:10.1007/s11692-022-09570-4 · Cited by 57 · see citing works
“These contingencies are also reflected by the finding that developmental simplicity evidently promotes evolvability in some situations, and we need a deeper analysis of how the predominant views on phenotypic modularity or dimensionality relate to the fact that bird beaks have more broadly diversified when underlain b…”
BackgroundPásztor, L., Botta‐Dukát, Z., Magyar, G., Czárán, T., & Meszéna, G. (2016) · doi:10.1093/acprof:oso/9780199577859.001.0001 · Cited by 85 · see citing works
Introgressive hybridization and natural selection in Darwin's finches
Grant, P. R., & Grant, B. R. (2015) · Biological Journal of the Linnean Society · doi:10.1111/bij.12702 · Cited by 54 · see citing works
“…strengthened by identified genes that influence the development of beak size and shape through the production of signalling molecules (Abzhanov et al., 2004, 2006; Mallarino et al., 2011), and by the variable effects of ALX1, a regulatory gene affecting beak shape (Lamichhaney et al., 2015).”
BackgroundSelf-citationGenetic and developmental basis for parallel evolution and its significance for hominoid evolution
Reno, P. L. (2014) · Evolutionary Anthropology Issues News and Reviews · doi:10.1002/evan.21417 · Cited by 53 · see citing works
Adaptive bill morphology for enhanced tool manipulation in New Caledonian crows
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The Genetic Basis of Rapidly Evolving Male Genital Morphology inDrosophila
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“…Werner et al. 2010; Wasik and Moczek 2011), echinoderms (Hinman and Davidson 2007), fish (Fraser et al. 2009), birds (Abzhanov et al. 2004, 2006; Mallarino et al. 2011), mammals (Cretekos et al. 2008), as well as morphological differences between Copyright © 2011 by the Genetics Society of…”
BackgroundBiogeography of species richness gradients: linking adaptive traits, demography and diversification
Carnicer, J., Brotons, L., Stefanescu, C., & Peñuelas, J. (2011) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.2011.00210.x · Cited by 52 · see citing works
“These genes and metabolic paths are possibly shared by most bird species and might become a powerful tool for the comparative study of morphological diversification (Wu et al., 2004; Abzhanov et al., 2004, 2006; Fitzpatrick et al., 2005, Campàs et al., 2010; Mallarino et al., 2011).”
BackgroundLundregan, S. L., Hagen, I. J., Gohli, J., Niskanen, A. K., Kemppainen, P., Ringsby, T. H., Kvalnes, T., Pärn, H., Rønning, B., Holand, H., et al. (2018) · Molecular Ecology · doi:10.1111/mec.14811 · Cited by 52 · see citing works
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Self-citationCraniofacial diversification in the domestic pigeon and the evolution of the avian skull
Young, N. M., Linde‐Medina, M., Fondon, J. W., Hallgrímsson, B., & Marcucio, R. (2017) · Nature Ecology & Evolution · doi:10.1038/s41559-017-0095 · Cited by 49 · see citing works
“These determinants are also thought to exhibit modularity 21 , in that they have independent effects on beak shape, consistent with our results.”
Implications of Developmental Gene Regulatory Networks Inside and Outside Developmental Biology
Peter, I. S., & Davidson, E. H. (2016) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2015.12.014 · Cited by 48 · see citing works
Parallel developmental genetic features underlie stickleback gill raker evolution
Glazer, A. M., Cleves, P. A., Erickson, P. A., Lam, A. Y., & Miller, C. T. (2014) · EvoDevo · doi:10.1186/2041-9139-5-19 · Cited by 48 · see citing works
“A classic set of phenotypes studied by evolutionary biologists are trophic traits, as many radiations (for example, Galapagos finches, African cichlids, threespine sticklebacks) display striking correlations between a population’s craniofacial pattern and the diet they eat [57-67].”
BackgroundRands, C. M., Darling, A. E., Fujita, M. K., Kong, L., Webster, M. T., Clabaut, C., Emes, R. D., Heger, A., Meader, S., Hawkins, M. B., et al. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-95 · Cited by 48 · see citing works
“Similar experiments elucidated the roles of three further developmental factors, Transforming Growth Factor beta Receptor Type II (TGFβRII), beta-Catenin (βCat) and Dickkopf-3 (Dkk3), at later stages of beak development that help in forming the bill shapes that are unique to ground finches [13].”
BackgroundSelf-citationThe adaptive genomic landscape of beak morphology in Darwin's finches
Lawson, L. P., & Petren, K. (2017) · Molecular Ecology · doi:10.1111/mec.14166 · Cited by 48 · see citing works
“Several of these a priori candidates were known to be components of complex developmental pathways (Abzhanov et al., 2004 p. 4, 2006; Mallarino et al., 2011), so it is perhaps not surprising that up and down regulation for shape change may be accomplished at various levels in these gene interaction…”
BackgroundInfluentialAbzhanov, A. (2017) · Development · doi:10.1242/dev.137505 · Cited by 45 · see citing works
“Other developmental genes, such as CaM, TGFβIIr, β-catenin and Dkk3 form a regulatory network and together explain other scaling parameters, such as beak length or width (Abzhanov et al., 2004, 2006; Mallarino et al., 2011, 2012) (Fig.”
BackgroundSelf-citationDevelopmental basis of phenotypic integration in two Lake Malawi cichlids
Pabic, P. L., Cooper, W. J., & Schilling, T. F. (2016) · EvoDevo · doi:10.1186/s13227-016-0040-z · Cited by 46 · see citing works
On the role of sparseness in the evolution of modularity in gene regulatory networks
Espinosa‐Soto, C. (2018) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1006172 · Cited by 45 · see citing works
Li, B., & Kimmel, M. (2013) · Genetics · doi:10.1534/genetics.113.154161 · Cited by 44 · see citing works
Square, T. A., Jandzík, D., Cattell, M. V., Coe, A., Doherty, J., & Medeiros, D. M. (2014) · Developmental Biology · doi:10.1016/j.ydbio.2014.10.016 · Cited by 43 · see citing works
“Recent work suggests that differences in the intercellular signals emanating from cranial epithelia can explain differences in skeletal element size and shape between closely related species (Abzhanov et al., 2004; Mallarino et al., 2011, 2012).”
BackgroundCadena, C. D., & Zapata, F. (2021) · The Auk · doi:10.1093/ornithology/ukaa069 · Cited by 43 · see citing works
Paths Less Traveled: Evo-Devo Approaches to Investigating Animal Morphological Evolution
Mallarino, R., & Abzhanov, A. (2012) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-101011-155732 · Cited by 42 · see citing works
“…in a group, which is not amenable to artificial breeding and direct genetic mapping, comparative analysis methods were employed, including the immunohistochemistry-based candidate gene approach, complementary DNA microarray screens, and qRT-PCR (Abzhanov et al. 2004, 2006; Mallarino et al. 2011).”
InfluentialSelf-citationPeramorphosis, an evolutionary developmental mechanism in neotropical bat skull diversity
Camacho, J. J., Heyde, A., Bhullar, B.-A. S., Haelewaters, D., Simmons, N. B., & Abzhanov, A. (2019) · Developmental Dynamics · doi:10.1002/dvdy.90 · Cited by 40 · see citing works
Self-citationFeeding innovations in a nested phylogeny of Neotropical passerines
Lefebvre, L., Ducatez, S., & Audet, J. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0188 · Cited by 39 · see citing works
Creating diversity in mammalian facial morphology: a review of potential developmental mechanisms
Usui, K., & Tokita, M. (2018) · EvoDevo · doi:10.1186/s13227-018-0103-4 · Cited by 40 · see citing works
Towards a Dynamic Interaction Network of Life to unify and expand the evolutionary theory
Bapteste, E. P., & Huneman, P. (2018) · BMC Biology · doi:10.1186/s12915-018-0531-6 · Cited by 40 · see citing works
Geometry and dynamics link form, function, and evolution of finch beaks
al-Mosleh, S., Choi, G. P. T., Abzhanov, A., & Mahadevan, L. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2105957118 · Cited by 37 · see citing works
Self-citationMolecular and cellular mechanisms underlying the evolution of form and function in the amniote jaw
Woronowicz, K. C., & Schneider, R. A. (2019) · EvoDevo · doi:10.1186/s13227-019-0131-8 · Cited by 34 · see citing works
Model species in evo‐devo: a philosophical perspective
Bolker, J. A. (2014) · Evolution & Development · doi:10.1111/ede.12056 · Cited by 34 · see citing works
“…groups that exemplify interesting evolutionary variations in development between sister taxa (Abzhanov et al. 2006; Cresko et al. 2006; Haag 2009; Mallarino et al. 2011; Manceau et al. 2011; Tautz 2011; Rajakumar et al. 2012; Sanger et al. 2012), or that are reasonable proxies for lineages…”
BackgroundMethodInfluentialSynergism of Natural Selection and Introgression in the Origin of a New Species
Grant, P. R., & Grant, B. R. (2014) · The American Naturalist · doi:10.1086/675496 · Cited by 35 · see citing works
“Some of the genes have been identified by our collaborators, Cliff Tabin, Arhat Abzhanov, and Ricardo Mallarino (Abzhanov et al. 2004, 2006; Mallarino et al. 2011).”
BackgroundSelf-citationMacroevolutionary and morphofunctional patterns in theropod skulls: a morphometric approach
Foth, C., & Rauhut, O. W. M. (2012) · Acta Palaeontologica Polonica · doi:10.4202/app.2011.0145 · Cited by 35 · see citing works
“However, this mor− phological variation seems to be controlled by only a small set of signal molecules ( −catenin, BMP, calmudulin, Dkk3, TGF IIr; Abzhanov et al. 2004, 2006; Wu et al. 2004, 2006; Mallarino et al. 2011).”
BackgroundThe patterns and modes of the evolution of disparity in Mesozoic birds
Wang, M., Lloyd, G. T., Zhang, C., & Zhou, Z. (2021) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2020.3105 · Cited by 31 · see citing works
“This pattern to some degree echoes the radiation of the iconic Darwin’s finches that is manifested largely by changes in beak form rather than limb proportions [48,49].”
BackgroundFeeding in Birds: Thriving in Terrestrial, Aquatic, and Aerial Niches
Rico‐Guevara, A., Sustaita, D., Gussekloo, S. W. S., Olsen, A. M., Bright, J. A., Corbin, C. E., & Dudley, R. (2019) · Fascinating life sciences · doi:10.1007/978-3-030-13739-7_17 · Cited by 33 · see citing works
“…to note that distinct sets of genes guiding the development of the prenasal cartilages (e.g., Bmp4, CaM) and premaxillary bones (TGFβIIr, β-catenin, and Dkk3) ultimately control different dimensions (Mallarino et al. 2011), and thereby enable a great diversity of shapes, sizes, and functions.”
BackgroundA Cross-Species Analysis of MicroRNAs in the Developing Avian Face
Powder, K. E., Ku, Y.-C., Brugmann, S. A., Veile, R. A., Renaud, N., Helms, J. A., & Lovett, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035111 · Cited by 32 · see citing works
“beak morphology [2,3,8,9,10,20], and it is very likely that many more mRNAs differ across this developmental window, miRNAs”
BackgroundEvo-devo beyond morphology: from genes to resource use
Irschick, D. J., Albertson, R. C., Brennan, P. L. R., Podos, J., Johnson, N., Patek, S. N., & Dumont, E. R. (2013) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2012.12.004 · Cited by 32 · see citing works
Lencer, E. S., Warren, W. C., Harrison, R., & McCune, A. R. (2017) · BMC Genomics · doi:10.1186/s12864-017-3810-7 · Cited by 31 · see citing works
“Other genes of note include slc24a4 (associated with enamel formation in human) [55], smoc1 (associated with craniofacial morphology in human) [56, 57], lbh (craniofacial evolution in cichlids) [58], ednrb (endothelin signaling) [59, 60], bambi (Bmp signaling and differential expression during bone remodeling) [61], a…”
BackgroundChauhan, B. K., Plageman, T. F., Lou, M., & Lang, R. A. (2015) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2014.11.011 · Cited by 29 · see citing works
“…the huge complexity of tissue shapes in different species and different organs teaches us that in morphogenesis, details and subtlety matter (an interesting example is the subtle changes in beak shape that allow “Darwin’s finches” to effectively exploit an ecological niche; Mallarino et al., 2011).”
BackgroundEvolutionary trade-offs and the structure of polymorphisms
Sheftel, H., Székely, P., Mayo, A., Sella, G., & Alon, U. (2018) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2017.0105 · Cited by 29 · see citing works
Evolution of beak morphology in the Ground Tit revealed by comparative transcriptomics
Cheng, Y., Gao, B., Wang, H., Han, N., Shao, S., Wu, S., Song, G., Zhang, Y. E., Zhu, X., Lü, X., et al. (2017) · Frontiers in Zoology · doi:10.1186/s12983-017-0245-6 · Cited by 29 · see citing works
Lee, H. W., Esteve‐Altava, B., & Abzhanov, A. (2020) · Scientific Reports · doi:10.1038/s41598-020-73083-3 · Cited by 28 · see citing works
Self-citationMechanisms of bacterial morphogenesis: Evolutionary cell biology approaches provide new insights
Jiang, C., Caccamo, P. D., & Brun, Y. V. (2015) · BioEssays · doi:10.1002/bies.201400098 · Cited by 28 · see citing works
Neural crest cells as a source of microevolutionary variation
Brandon, A. A., Almeida, D., & Powder, K. E. (2022) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2022.06.001 · Cited by 26 · see citing works
Knief, U., Schielzeth, H., Kempenaers, B., Ellegren, H., & Forstmeier, W. (2012) · Molecular Ecology · doi:10.1111/j.1365-294x.2012.05661.x · Cited by 26 · see citing works
“The other significant QTL peak region for beak width on chromosome Tgu2 harbours three candidate genes (CTNNB1, SHH and TGFBR2), but none of them is known to influence beak width.”
BackgroundInfluentialHistorical museum samples enable the examination of divergent and parallel evolution during invasion
Stuart, K. C., Sherwin, W. B., Austin, J. J., Melissa Bateson, B., Eens, M., Brandley, M. C., & Rollins, L. A. (2022) · Molecular Ecology · doi:10.1111/mec.16353 · Cited by 25 · see citing works
“…established as a top candidate gene for regulating differential beak morphology, and functional alterations in this gene are commonplace across many avian species (Abzhanov et al., 2006; Knief et al., 2012; Mallarino et al., 2011), suggesting a possible rapid response to changes in food source.”
BackgroundHuman genetic variation within neural crest enhancers: molecular and phenotypic implications
Rada-Iglesias, A., Prescott, S. L., & Wysocka, J. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0360 · Cited by 24 · see citing works
Pallares, L. F., Turner, L. M., & Tautz, D. (2016) · Development Genes and Evolution · doi:10.1007/s00427-016-0550-7 · Cited by 24 · see citing works
“Several studies have explored craniofacial shape variation between subspecies of the house mouse (Mus musculus) around the world (Macholán 2006; Boell and Tautz 2011; Siahsarvie et al. 2012).”
BackgroundComparative Genomics and Evolution of Avian Specialized Traits
Wu, L., Jiao, X., Zhang, D., Cheng, Y., Song, G., Qu, Y., & Lei, F. (2021) · Current Genomics · doi:10.2174/1389202923666211227143952 · Cited by 23 · see citing works
“Previous studies have shown that the expression of BMP4 [57], CALM1 [58], TGFBR2 [59], CTNNB1 [59], DKK3 [59], and some other genes are related to the size and shape of beaks.”
ResultCheek, R. G., Forester, B. R., Salerno, P. E., Trumbo, D. R., Langin, K. M., Chen, N. X., Sillett, T. S., Morrison, S. A., Ghalambor, C. K., & Funk, W. C. (2022) · Molecular Ecology · doi:10.1111/mec.16438 · Cited by 21 · see citing works
“…in pathways associated with bill morphology (Abzhanov et al., 2004, 2006; Badyaev et al., 2008; Bosse et al., 2017; Lundregan et al., 2018; Mallarino et al., 2011) including bone morphogenetic protein (SMURF1; BMP15), ossification (PBX1), calmodulin (IQCB1; PPP3CB; HSPA2), Smad proteins…”
BackgroundCooper, W. J., Wirgau, R. M., Sweet, E. M., & Albertson, R. C. (2013) · Evolution & Development · doi:10.1111/ede.12052 · Cited by 22 · see citing works
“…(e.g., African cichlid fishes, Darwin’s finches, Damselfishes, and Mammals; Cooper and Westneat 2009; Cooper et al. 2010; Goswami et al. 2011; Mallarino et al. 2011), studies of the controls of skull morphogenesis are critical for establishing the ontogenetic underpinnings of evolutionary…”
BackgroundGross, J. B., Stahl, B. A., Powers, A. K., & Carlson, B. M. (2015) · Evolution & Development · doi:10.1111/ede.12131 · Cited by 20 · see citing works
“Genetic studies using Darwin’s finches (Mallarino et al. 2011), teleost fish (Hulsey et al.”
BackgroundDroguett, D. H. P., & Kronforst, M. R. (2015) · BioEssays · doi:10.1002/bies.201500047 · Cited by 20 · see citing works
“domains of expression of these candidate genes correlated with adult morphology and that the genes interact to determine different axes of growth [39].”
BackgroundGenome size drives morphological evolution in organ‐specific ways
Itgen, M. W., Natalie, G. R., Siegel, D. S., Sessions, S. K., & Mueller, R. L. (2022) · Evolution · doi:10.1111/evo.14519 · Cited by 20 · see citing works
“of diffusion and biochemical reactions; morphology and motility of cells; rates of cellular division and differentiation; and the size and organization of tissues and structures (Alberch, 1983; Brakefield et al., 2003; Mallarino et al., 2011; Keyte and Smith, 2014; Powder et al., 2015).”
BackgroundPritchard, V. L., Viitaniemi, H. M., McCairns, R. J. S., Merilä, J., Nikinmaa, M., Primmer, C. R., & Leder, E. H. (2017) · G3 Genes Genomes Genetics · doi:10.1534/g3.116.033241 · Cited by 19 · see citing works
Craniofacial development illuminates the evolution of nightbirds (Strisores)
Navalón, G., Nebreda, S. M., Bright, J. A., Fabbri, M., Benson, R., Bhullar, B.-A. S., Marugán‐Lobón, J., & Rayfield, E. J. (2021) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2021.0181 · Cited by 21 · see citing works
Biological Interfaces, Modulation, and Sensing with Inorganic Nano‐Bioelectronic Materials
Schaumann, E. N., & Tian, B. (2020) · Small Methods · doi:10.1002/smtd.201900868 · Cited by 19 · see citing works
A ROR2 coding variant is associated with craniofacial variation in domestic pigeons
Boer, E. F., Hollebeke, H. F. V., Maclary, E. T., Holt, C., Yandell, M. D., & Shapiro, M. D. (2021) · Current Biology · doi:10.1016/j.cub.2021.08.068 · Cited by 17 · see citing works
Allometric conservatism in the evolution of bird beaks
Rombaut, L. M. K., Capp, E. J. R., Cooney, C. R., Hughes, E. C., Varley, Z. K., & Thomas, G. H. (2021) · Evolution Letters · doi:10.1002/evl3.267 · Cited by 18 · see citing works
“Although progress has been made in our understanding of the genetic-developmental basis of variation in bird beak size and shape (Grant et al. 2006; Mallarino et al. 2011, 2012), more research is necessary to understand the mechanistic basis of constraints on the independent evolution of the beak…”
BackgroundSimon, M. N., Brandt, R., Kohlsdorf, T., & Arnold, S. J. (2019) · Biological Journal of the Linnean Society · doi:10.1093/biolinnean/blz067 · Cited by 18 · see citing works
Neural Crest Cells in Craniofacial Skeletal Development
Schilling, T. F., & Pabic, P. L. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-401730-6.00008-9 · Cited by 18 · see citing works
Asymmetric requirement of surface epithelial β‐catenin during the upper and lower jaw development
Sun, Y., Teng, I., Huo, R., Rosenfeld, M. G., Olson, L. E., Li, X., & Li, X. (2012) · Developmental Dynamics · doi:10.1002/dvdy.23755 · Cited by 17 · see citing works
“have been implicated in the evolutionary adaptations and variations of species-specific facial appearances (Brugmann et al., 2007; Mallarino et al., 2011).”
Background
- 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
- Physical Sciences › Mathematics › Geometry and Topology › Morphological variations and asymmetry
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › 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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