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Xenopus) Tropicalis Dentition The Developmental Basis of Variation in Tooth and Jaw Patterning: Evolved Differences in the Silurana (Xenopus) tropicalis Dentition By Theresa Marie Grieco A dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Integrative Biology in the Graduate Division of the University of California, Berkeley Committee in charge: Professor Leslea J. Hlusko, Chair Professor Marvalee H. Wake Professor Anthony D. Barnosky Professor Craig T. Miller Fall 2013 The Developmental Basis of Variation in Tooth and Jaw Patterning: Evolved Differences in the Silurana (Xenopus) tropicalis Dentition Copyright © 2013 by Theresa Marie Grieco Abstract The Developmental Basis of Variation in Tooth and Jaw Patterning: Evolved Differences in the Silurana (Xenopus) tropicalis Dentition by Theresa Marie Grieco Doctor of Philosophy in Integrative Biology University of California, Berkeley Professor Leslea Hlusko, Chair Perhaps the most evident conversion of genomic information into functional, morphological phenotypes in an animal occurs during organogenesis, and the study of vertebrate tooth development provides a phenotypically diverse system for which the mechanisms for patterning and morphogenesis have been extensively studied. An understanding of the developmental basis for evolved differences between teeth in different anatomical and phylogenetic contexts brings complementary information to our knowledge of odontogenic mechanisms. Examining difference, or variation, allows for the validation of hypothesized developmental mechanisms, identification of mechanistic flexibility that could be available to evolution or bioengineering, and the redefinition of phenotypes to better align with the natural biological variation available. This dissertation examines the development of the dentition in the frog and emerging developmental model Silurana (Xenopus) tropicalis, including the first gene expression data for odontogenesis in any amphibian. Comparative data for the evolution of dental phenotypes are assembled from descriptions of tooth initiation, dentition patterning, and adult craniodental variation phenotypes, addressing developmental questions at population, subfamily, and phylum levels. Using hematoxylin and eosin-stained histological sections and whole mount preparations of larval S. tropicalis jaws, I demonstrate that individual tooth initiation is broadly similar to that documented for phylogenetic relative Xenopus laevis, but that the process is temporally shifted relative to external developmental traits in the Nieuwkoop and Faber staging system. Furthermore, patterns of tooth initiation in S. tropicalis reveal a lack of synchrony in alternating tooth positions and dynamics that were previously undetected. The frequent presence of ‘twinned’ tooth germs in whole mount preparations argues against a robust model of local inhibition directing tooth initiation in this species. These findings rule out two hypothesized developmental mechanisms for tooth initiation in S. tropicalis that were derived from data in X. laevis and other homodont vertebrates. In another investigation of first generation tooth development, I examine the expression of Sonic hedgehog (Shh), a marker for several phases of odontogenesis across vertebrates. I demonstrate 1 the utility of comparing ‘natural experiments’ in development with what is known from more anatomically conservative developmental models. In particular, I use the fact that S. tropicalis teeth do not initiate until just before metamorphosis as a case where tooth formation and mouth formation developmental programs are dissociated from one another to evaluate the current consensus odontogenic model for Shh. With in situ hybridization data from S. tropicalis, I fail to detect a Shh-expressing odontogenic band prior to tooth formation, counter to predictions from the consensus model. A review of published functional data and the correspondence between an odontogenic band domain and the presence of functional teeth in other vertebrates reveal several other taxa for which the consensus model appears insufficient to account for variation in the distribution of the marginal dentition. Finally, I explore the ability to infer developmental processes from patterns of adult craniodental variation in three S. tropicalis genetic strains raised in captivity. Osteological measurements and tooth counts are analyzed for patterns of covariation at the functional phenotypic levels of the cranium, the jaw, and the tooth-bearing bone. I demonstrate that the bimodal sexual body length dimorphism does not carry over to any cranial metric trait measured; systemic factors affecting cranial length can explain much of the difference between male and female traits, which are distributed unimodally. Patterns of covariation with cranial size, size-adjusted patterns of pairwise phenotypic correlation, and significant differences between genetic strains all suggest a relative independence of variation in the premaxilla and maxilla in S. tropicalis, and I document evidence for a functional jaw module, in which the tooth row and jaw bones correlate when summed across the jaw, but in which tooth and jaw phenotypes lack integration at the level of individual tooth-bearing bones. 2 TABLE OF CONTENTS TABLE OF CONTENTS ………………………………………………………………...……… i LIST OF FIGURES AND TABLES …………………………………………………………… iii DEDICATION ………………………………………………………………………….………. iv ACKNOWLEDGMENTS ………………………………………………………………………. v CURRICULUM VITAE ………………………………………………………….……………. vii INTRODUCTION ………………………………………………………………………………. 1 A conserved developmental mechanism employed in different contexts ……………….. 2 Odontogenesis in the frog Silurana (Xenopus) tropicalis ……………………………….. 3 An integrative approach to S. tropicalis odontogenesis …………………………………. 4 References ……………………………………………………………………………..… 6 CHAPTER 1: Tooth initiation in Silurana (Xenopus) tropicalis reveals dynamic patterning of the first tooth generation …………………………………………………………………………… 14 Abstract ……………………………………………………………………………….... 14 Introduction ……….……………………………………………………………………. 14 Materials and Methods ……………….……………………………………………….... 16 Results and Discussion .…………………………………………………………..……. 18 Individual tooth morphogenesis ……………………………………………...… 18 First generation teeth ………………………………………………………..….. 18 Heterochrony in the onset of tooth initiation ………………………………...… 20 Initiation patterns in the upper jaw …………………………………………….. 21 Triggers for tooth development ………………………………………..………. 22 Initiation patterns across vertebrates …………………………………………… 24 Conclusions ……………………………………………………………………..……… 24 References ………………………………………………………………………...……. 26 CHAPTER 2: Shh gene expression in S. tropicalis teeth and a re-evaluation of the vertebrate odontogenic band ………………………………………………………………………………. 37 Abstract ……………………………………………………………………………….... 37 Introduction …………………………………………………………………………….. 37 The consensus model for odontogenesis as marked by Shh ………………….... 38 Reasons to question Shh function in the consensus model of tooth initiation …. 39 A comparative approach as a test of the consensus model …………………..… 40 Materials and Methods ....……………………………………………………………..... 41 Results ………………………………………………………………………………….. 42 Shh gene expression in S. tropicalis …………………………………..……….. 42 Shh is not detected in odontogenic band or placodes stages ……….…... 43 Shh is expressed in the IDE of late-developing first generation teeth …. 43 Evaluating the phenotypic definition of the odontogenic band ………………... 44 Discrepancies between Shh-defined OB and tooth formation ………..... 44 The OB is not sufficient to fully form teeth ……………….…… 44 The OB is not necessary for most of the tooth developmental program to occur ……………………………………………….. 46 i Temporal context of the OB ……………………………………………..…….. 47 Precursors of tooth development: The stomodeum ……………….…… 47 Precursors of tooth development: Shh in craniofacial patterning ……… 49 Summary and Discussion ………………………………………………………...…….. 49 Differences in frog odontogenesis provide insights into tooth initiation ………. 50 Phenotypic correlates of the OB: What is functional in tooth induction/competence? ……………………………………………………….... 51 Conclusions …………………………………………………………………..………… 52 References ……………………………………………………………………………… 54 CHAPTER 3: Sex, size, and development: Narrowing down influences on adult craniodental variation in Silurana (Xenopus) tropicalis ………………………………………………..……. 68 Abstract ………………………………………………………………………...………. 68 Introduction ………………………………………………………………………......… 68 Systemic influences: Body size …...………………………………………....… 69 Systemic influences: Sexual dimorphism ………………...……………………. 70 Local influences ………………………………………………………………... 72 Materials and Methods .……………………………………………………………..….. 73 Results ………………………………………………………………………………….. 75 Systemic influences ……………………………………………………………. 75 Body size dimorphism: convoluting size and sex …………………...…. 75 Cranial size and shape ……………………………………..……...……. 75 Localized effects of systemic influences …………………………………….… 76 Sex and size effects isolated to the cranium ………………………..….. 76 Size effects in the dentition …………………………………………….. 77 Morphological integration in the cranium ……………………..………. 77 Local influences …………………………………………………………….….. 78 Submodules within the cranium ………………………………...……… 78 Developmental remnants in adult variation ……………………………. 79 Decoupled maxillary tooth row and jaw bone phenotypes …………….. 79 Sutures and functional tooth positions …………………………………. 80 Genetic basis for craniodental variation ……………………………………….. 81 Discussion ……………………………………………………………………………...
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