title: Closely related bird species demonstrate flexibility between beak morphology and underlying developmental programs.
abstract: The astonishing variation in the shape and size of bird beaks reflects a wide range of dietary specializations that played an important role in avian diversification. Among Darwin's finches, ground finches (Geospiza spp.) have beaks that represent scaling variations of the same shape, which are generated by alterations in the signaling pathways that regulate growth of the two skeletal components of the beak: the prenasal cartilage (pnc) and the premaxillary bone (pmx). Whether this developmental mechanism is responsible for variation within groups of other closely related bird species, however, has remained unknown. Here, we report that the Caribbean bullfinches (Loxigilla spp.), which are closely related to Darwin's finches, have independently evolved beaks of a novel shape, different from Geospiza, but also varying from each other only in scaling. However, despite sharing the same beak shape, the signaling pathways and tissues patterning Loxigilla beaks differ among the three species. In Loxigilla noctis, as in Geospiza, the pnc develops first, shaped by Bmp4 and CaM signaling, followed by the development of the pmx, regulated by TGFβIIr, β-catenin, and Dkk3 signaling. In contrast, beak morphogenesis in Loxigilla violacea and Loxigilla portoricensis is generated almost exclusively by the pmx through a mechanism in which Ihh and Bmp4 synergize to promote expansion of bone tissue. Together, our results demonstrate high flexibility in the relationship between morphology and underlying developmental causes, where different developmental programs can generate identical shapes, and similar developmental programs can pattern different shapes.
authors.affiliation: Department of Organismic and Evolutionary Biology and School of Engineering and Applied Sciences, Harvard University, Cambridge, MA 02138, USA.
authors.forename: Ricardo
authors.initials: R
authors.lastname: Mallarino
authors.forename: Otger
authors.initials: O
authors.lastname: Campàs
authors.forename: Joerg A
authors.initials: JA
authors.lastname: Fritz
authors.forename: Kevin J
authors.initials: KJ
authors.lastname: Burns
authors.forename: Olivia G
authors.initials: OG
authors.lastname: Weeks
authors.forename: Michael P
authors.initials: MP
authors.lastname: Brenner
authors.forename: Arhat
authors.initials: A
authors.lastname: Abzhanov
mesh_terms: D000818:Animals; D001483:Base Sequence; D001499:Bayes Theorem; D001502:Beak / Q000033:anatomy & histology / Q000196:embryology*; D005075:Biological Evolution; D055415:Bone Morphogenetic Protein 4 / Q000378:metabolism; D002147:Calmodulin / Q000378:metabolism; D002356:Cartilage / Q000196:embryology; D002642:Chick Embryo; D005147:Facial Bones / Q000196:embryology; D046369:Finches / Q000196:embryology* / Q000235:genetics*; D053823:Hedgehog Proteins / Q000378:metabolism; D007150:Immunohistochemistry; D017403:In Situ Hybridization; D008957:Models, Genetic; D008969:Molecular Sequence Data; D009024:Morphogenesis / Q000502:physiology*; D010802:Phylogeny; D018125:Receptors, Transforming Growth Factor beta / Q000378:metabolism; D017422:Sequence Analysis, DNA; D015398:Signal Transduction / Q000502:physiology*; D013045:Species Specificity; D051176:beta Catenin / Q000378:metabolism
chemical_list: D055415:Bone Morphogenetic Protein 4; D002147:Calmodulin; D053823:Hedgehog Proteins; D018125:Receptors, Transforming Growth Factor beta; D051176:beta Catenin