Molecular and Cellular Mechanisms Underlying the Evolution of Form and Function in the Amniote Jaw Katherine C

Woronowicz and Schneider EvoDevo (2019) 10:17 https://doi.org/10.1186/s13227-019-0131-8 EvoDevo REVIEW Open Access Molecular and cellular mechanisms underlying the evolution of form and function in the amniote jaw Katherine C. Woronowicz1,2 and Richard A. Schneider1* Abstract The amniote jaw complex is a remarkable amalgamation of derivatives from distinct embryonic cell lineages. During development, the cells in these lineages experience concerted movements, migrations, and signaling interactions that take them from their initial origins to their fnal destinations and imbue their derivatives with aspects of form including their axial orientation, anatomical identity, size, and shape. Perturbations along the way can produce defects and disease, but also generate the variation necessary for jaw evolution and adaptation. We focus on molecular and cellular mechanisms that regulate form in the amniote jaw complex, and that enable structural and functional integration. Special emphasis is placed on the role of cranial neural crest mesenchyme (NCM) during the species-specifc patterning of bone, cartilage, tendon, muscle, and other jaw tissues. We also address the efects of biomechanical forces during jaw development and discuss ways in which certain molecular and cellular responses add adaptive and evolutionary plasticity to jaw morphology. Overall, we highlight how variation in molecular and cellular programs can promote the phenomenal diversity and functional morphology achieved during amniote jaw evolution or lead to the range of jaw defects and disease that afect the human condition. Keywords: Amniote jaw development and evolution, Form and function, Neural crest, Secondary cartilage, Mechanical environment Introduction Additionally, while most amniote jaws are bilaterally Te jaws of amniotes display a marvelous array of sizes symmetrical, snail-eating snakes (i.e., Pareas) have bro- and shapes, and there are countless examples of how the ken the symmetry of the dentition on their mandibles form of the jaws has evolved to function in every con- and develop more teeth on the right side as a means to ceivable ecological niche [1–7]. One obvious purpose for prey upon clockwise-coiled (dextral) snails [9, 10]. Simi- the jaw apparatus is to obtain, manipulate, process, and larly, among birds, crossbills (i.e., Loxia) have bilaterally ingest dietary items. For instance, among reptiles, many and dorsoventrally asymmetrical beaks such that the snakes often consume prey larger than their own skulls distal tips traverse one another. Te lower jaw crosses to and can accommodate extreme expansion with highly the left or right side with equal frequencies in crossbill fexible upper and lower jaws. Large prey is incremen- populations [11] and this unusual adaptive co-evolution tally forced down the esophagus by “snout shifting” or permits these birds to pry open conifer cone scales and “pterygoid walking” in which tooth-bearing elements extract seeds [12, 13]. Within mammals, giant anteaters of the upper jaw alternately ratchet over the prey [8]. (i.e., Myrmecophaga), which retrieve insects from tightly confned spaces like insect burrows, have evolved a specialized ability to “open” their jaws by rotating their man- *Correspondence: [email protected] 1 Department of Orthopaedic Surgery, University of California at San dibles along the long axis rather than by depressing the Francisco, 513 Parnassus Avenue, S-1161, Box 0514, San Francisco, CA mandibles [14]. Tese are but a few extreme examples of 94143-0514, USA what amniotes have accomplished with their jaws. Full list of author information is available at the end of the article © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/ publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Woronowicz and Schneider EvoDevo (2019) 10:17 Page 2 of 21 Yet while myriad jaw morphologies exist today and in ectoderm, mesoderm, endoderm), but especially the cra- the fossil record, all amniote jaws share common devel- nial neural crest mesenchyme (NCM), which is a major opmental and evolutionary origins, and their form and contributor to the jaws, must communicate seamlessly function are typically achieved by integrating many of to produce a musculoskeletal system that is structur- the same adjoining skeletal, muscular, nervous, vascu- ally integrated in support of its normal and often highly lar, and connective tissue components [15, 16]. How specialized use. Achieving such species-specifc form then does the species-specifc form of the jaws emerge and function in the jaws is a dynamic multidimensional in development and change during evolution in relation problem that embryos have to solve [37]. In particular, to function? In particular, what molecular and cellular there need to be mechanisms in place facilitating the spe- mechanisms pattern the jaws of embryos in a manner cies-specifc modulation of parameters such as cell cycle that anticipates later adult use and promotes adaptation? length, cell size, cell number, cell specifcation, cell fate, Tese are fundamental questions in biology and there is a cell diferentiation, and more [7, 38–43]. Teasing apart long history of eforts to answer them using the jaw com- such mechanisms as well as those underlying the migra- plex as a subject of study. tion, distribution, and interactions among jaw precur- Early attempts to link form and function in the jaws sor populations (Fig. 1a), and also identifying the critical as well as the skull more broadly began at the gross ana- signals through which these cells acquire and implement tomical level. Meticulous descriptions conducted in a their axial orientation, anatomical identity, and tissue transcendental and pre-evolutionary framework such as type, is essential for understanding how the jaws become those from Goethe, Oken, Dumeril, Geofroy, Owen, and patterned and structurally integrated. By applying mod- many others laid the foundation for comparative methods ern experimental strategies, the molecular and cellular to study morphological variation and adaptation [17–19]. events that underlie jaw form and function during devel- Describing form and function among animals required opment, disease, and evolution are being elucidated. special language, and Owen coined, “homology” and Some of these studies and their key insights are reviewed “analogy” with this goal in mind. Such concepts facili- in the sections below. tated discussions about the structural plan for vertebrates and whether cranial elements being compared across Anatomical organization and integration of the jaw taxa were indeed “the same organ in diferent animals apparatus under every variety of form and function” [20, p. 379]. In Te head skeleton has classically been organized into line with the transcendentalists before him, Owen pos- three compartments each with distinct embryological tulated that the vertebrate skull and its constituent parts and evolutionary histories, anatomical locations, and like the jaws extended as a serial homolog of the trunk various degrees of structural and functional integration: skeleton [21, 22]. Owen’s ideas impacted the way the con- the neurocranium, viscerocranium, and dermatocranium cept of homology and the anatomy of the cranial com- (Fig. 1b) [3, 15, 19, 44–47]. Te neurocranium has been plex were viewed and debated for years thereafter [3, 19, defned as the skeleton that primarily forms frst as car- 23–33]. During the nineteenth century, questions of form tilage and surrounds the brain and sense organs. Te vis- and function became rooted in comparative embryology, cerocranium (or “splanchnocranium”) has been viewed especially around the anatomical discoveries of workers as the cartilaginous skeleton of the jaws and of the seri- like Rathke, Reichert, and Huxley, and the proposed laws ally repeated arches in the pharyngeal region of the gut of Haeckel [16, 18, 34, 35]. For example, Haeckel used tube. Te neurocranium and viscerocranium are thought his observations on the pharyngeal arches of various to have evolved as part of a vertebrate endoskeleton [3, embryos to help explain how ontogeny could connect the 22, 48–50]. In contrast, the dermatocranium has been forms of animals in a phylogenetic progression. Although described as a component of the vertebrate exoskeleton, Haeckel and his followers concluded rather erroneously which in the skull consists of the palatal, cranial vault, that “ontogeny recapitulates phylogeny” [36], such early and tooth-bearing elements around the oral cavity [46, work built a vocabulary and an intellectual framework 51–54]. Moreover, these skeletal systems have divergent through which the mechanisms of structural and func- embryonic origins in terms of cell lineages and process of tional integration in the head could be probed for almost diferentiation [19, 37, 47, 50, 55, 56]. 200 years and up to the present. In jawed vertebrates, the neurocranium and derma- Yet while the evolutionary history and comparative tocranium develop from dual mesenchymal lineages anatomy of the jaws have

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