Great Transformations in Vertebrate Evolution

Great Transformations in Vertebrate Evolution

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Great Transformations in Vertebrate Evolution by Kenneth P. Dial

How did flying birds evolve from running dinosaurs, terrestrial trotting tetrapods evolve from swimming fish, and whales return to swim in the sea? These are some of the great transformations in the 500-million-year history of vertebrate life. And with the aid of new techniques and approaches across a range of fields—work spanning multiple levels of biological organization from DNA sequences to organs and the physiology and ecology of whole organisms—we are now beginning to unravel the confounding evolutionary mysteries contained in the structure, genes, and fossil record of every living species.

This book gathers a diverse team of renowned scientists to capture the excitement of these new discoveries in a collection that is both accessible to students and an important contribution to the future of its field. Marshaling a range of disciplines—from paleobiology to phylogenetics, developmental biology, ecology, and evolutionary biology—the contributors attack particular transformations in the head and neck, trunk, appendages such as fins and limbs, and the whole body, as well as offer synthetic perspectives. Illustrated throughout, Great Transformations in Vertebrate Evolution not only reveals the true origins of whales with legs, fish with elbows, wrists, and necks, and feathered dinosaurs, but also the relevance to our lives today of these extraordinary narratives of change.

Product Details

ISBN-13: 9780226268392
Publisher: University of Chicago Press
Publication date: 07/20/2015
Sold by: Barnes & Noble
Format: NOOK Book
Pages: 424
File size: 24 MB
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About the Author

Kenneth P. Dial is professor of biology at the University of Montana and founding director of the university’s Flight Laboratory and Field Station at Fort Missoula. Neil Shubin is senior advisor to the president and the Robert R. Bensley Distinguished Service Professor of Anatomy at the University of Chicago. His books include The Universe Within: Discovering the Common History of Rocks, Planets, and People and Your Inner Fish: A Journey into the 3.5-Billion-Year History of the Human Body. Elizabeth L. Brainerd is professor of medical science and director of the XROMM Technology Development Project at Brown University.

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Great Transformations in Vertebrate Evolution

By Kenneth P. Dial, Neil Shubin, Elizabeth L. Brainerd

The University of Chicago Press

Copyright © 2015 The University of Chicago
All rights reserved.
ISBN: 978-0-226-26839-2


Origin of the Vertebrate Dentition: [Teeth Transform Jaws into a Biting Force

Moya Meredith Smith and Zerina Johanson


How did the great transformation from "jawless suckers" to the "predatory monsters" of the oceans occur, involving the evolution of organized dentitions and jaws? It might be expected that jaws and teeth evolved together, but both are considered as independent modules with separate developmental pathways and separate evolutionary origins.

The emphasis of this chapter is on the organization of dentitions (regulation of separate teeth into ordered sets), how they evolved, and how they are patterned in development. The origins of the vertebrate dentition are currently controversial, contrasting tooth origins in evolution either from internal denticles lining the gill arches (seen to be anatomically separate from bony gill rakers), or from external body denticles (scales). Essentially these theories consider how teeth became organized into functional dentitions, and discussion of these controversies will be the main focus of this chapter. An essential premise that we will develop is that structures like teeth and jaws evolve via co-option of existing developmental modules of other structures (e.g., gill arch denticles vs. external denticles), by tinkering with the developmental genes that are also co-opted with the module (e.g., Raff 1996; but see Kuratani 2012). First, however, we discuss the evolution of the vertebrate jaws, a topic of considerable research interest in recent years.

Evolution of Vertebrate Jaws

The vertebrate jaw and gill arches can be considered serially homologous structures (Gegenbaur 1878; Gillis et al. 2013); classically, jaw evolution was believed to involve a modification of the first two arches into the jaw, with all structures in the pharyngeal walls arranged as an iterative series (fig. 1.1A). The skeletal structures of the most anterior mandibular arch include a dorsal palatoquadrate articulating to a ventral Meckelian arch, with the functional jaw articulation including the second hyoid arch as support, also with dorsal and ventral elements (fig. 1.1A, C). This is a generalized arrangement found, for example, in sharks (fig. 1.1C, Squalus) where behind the jaws five dorsal and ventral paired pharyngeal cartilages (fig. 1.1B, C) are preserved. Support for the oral dentition is provided by the first two arches, while more posterior pharyngeal arches (three to five, or six) are cartilaginous gill supports, but may also support teeth (arch five) in fish with well-ordered pharyngeal teeth functioning in food processing (zebrafish, cichlids). These more posterior arches are internal to the gills and also jointed, with a rostral bend to the dorsal part, then reflexed (fig. 1.1B, C, E). These contrast with the branchial basket of extant jawless vertebrates such as the lamprey (with a mouth as a sucker with rings of keratinous toothlets, supported by a circular cartilage; fig. 1.1D, F), where the branchial basket cartilages surround the gill openings and are external to the gills, neither jointed nor reflected in a rostral to caudal direction (fig. 1.1D, G). However, the modern shark visceral skeleton also has an iterative set of extrabranchial cartilages (fig. 1.1C, E, blue), equivalent topographically and with a similar passive respiratory function (recoil) to the lamprey branchial basket (Mallatt 1996; fig. 1.1D, blue, acting as gill supports, but inner branchial arch cartilages are absent; cf. fig. 1.1E, G). Therefore, the iterative cartilages of the lamprey branchial basket cannot have given rise to the inner cartilages of the jaws and gill supports, because both coexist in the modern shark (extrabranchial cartilages homologous to the branchial basket; Mallatt 1996), establishing the condition for Patterson's congruence test for nonhomology (Patterson 1988).

Although the iterative nature of the jaws, pharyngeal arches, and associated structures is not in doubt, and these can be compared as serial homologues in each of the major clades of jawed vertebrates, the way in which jaws evolved is still a question being studied by several research groups. Whether any structures in the lamprey gave rise to mandibular and hyoid skeletons of the jaws in chondrichthyans and osteichthyans is the subject of active debate and new experimental data (cf. fig. 1.1C, D; see Kuratani 2012 for a summary). It is interesting that in de Beer's famous treatise on development of the vertebrate skull in the lamprey he showed paired medial structures that were thought to represent the mandibular and hyoid precursors of the cartilaginous jaws (fig. 1.1C1; from de Beer 1971: pl. 9-6; anlagen for mandibular [red] and hyoid [green] cartilages); in the adult they become the piston cartilages and support (fig. 1.1D, same coding as C1), but there are no caudal medial cartilages in series with them as gill supports (pink cartilage as in fig.1.1C, E).

In jawed vertebrates, development of the jaw cartilages and hyoid precedes that of the pharyngeal arches. Also, earlier work in the chick embryo (Veitch et al. 1999) has shown that in the serial organization of the pharyngeal arches (see figs. 1.1D, 1.2A for general organization of the jawless vertebrate pharyngeal region) neural crest-dependent and independent patterning mechanisms operate. The pharyngeal arches are regionalized and have a sense of identity, anteroposterior position in the pharynx, different from that of pharyngeal segmentation (such as pouches, fig. 1.2D, E), which predates in evolutionary terms the role of neural crest in this process that is largely contributing to the cartilaginous supports. This suggested that the serial, medial pharyngeal cartilaginous skeleton is a secondary evolutionary acquisition. Perhaps it can be proposed that the inner series of pharyngeal cartilages (medial) are a neomorphic evolutionary step (neural crest-dependent) modeled on the mandibular but in particular the hyoid arch, as an iteration of this structure, using the hyoid set of genes and developmental processes to make gill supports (fig. 1.1B, C, E). In some ways the ideas of Kuratani (2012) reflect this, as he suggests evolution of a new developmental program based on novel gene regulatory networks, assumed in the context of a stepwise evolution of jaw patterning. In the classic model (fig. 1.1A), putative jaw supports developed from the unmodified mandibular and hyoid arches, as anterior supports of the series in the pharynx that were proposed to have already existed in jawless vertebrates (see fig. 1.1C1, D); however, medial, iterative pharyngeal skeletal arches were absent. Consequently, these could not have given rise in evolution to the medial skeletal supports of the more anterior jaws and hyoid (cf. fig. 1.1E, G), hence their origin in evolution was proposed as from the existing, more rostral, medial arches (mandibular and hyoid, fig 1.1C1, D).

The evolution of developmental processes that gave rise to articulating jaws are very controversial and in need of developmental, experimental data, some of which is outlined here. Linking these iterative structures with molecular information about a proposed patterning mechanism, nested Hox genes provide anterior-posterior positional information to the gill arches, and determine their identity, but are absent from the first arch (jaw) (Cohn 2002), and, intriguingly, also from the first pharyngeal arch in lampreys (Takio et al. 2007). Homeobox genes such as the Dlx family have been implicated in the dorsal-ventral patterning of gill arches, while Bapx1 and Gdf5/6/7 are involved in joint development (Depew et al. 2002, 2005; Cerny et al. 2010; Kuraku et al. 2010; Gillis et al. 2013; Takechi et al. 2013). Nested Dlx genes are present in jawed vertebrates (dlx1, 2 expressed dorsally in all arches, dlx1–6 ventrally, dlx1, 2, 5, 6 expressing in an intermediate position; Gillis et al. 2013), and have also been identified in lampreys (Cerny et al. 2010), however, whether these dlx genes are orthologous to hose in jawed vertebrates remains uncertain (Gillis et al. 2013; Takechi et al. 2013). Bapx1 was also absent from the lamprey arches (Cerny et al. 2010).

Researchers studying jaw evolution have focused on comparisons between living jawless vertebrates such as the lamprey and living jawed vertebrates. However, there are several groups of fossil jawed vertebrates that are more closely related to extant jawed vertebrates, including the Galeaspida and Osteostraci. New nondestructive methods, such as synchrotron radiation X-ray tomographic microscopy, are now available to study the internal anatomy of these fossils in substantial detail, providing crucial data on the question of jaw evolution. One current theory, the "heterotopy theory of jaw evolution," developed by Shigeru Kuratani and his colleagues suggests that the jaw evolved via a posterior (heterotopic) shift of the genes involved in jaw development and the change from monorhyny (single dorsal nasohypophyseal opening) to the diplorhyny (two nasal openings and a separate hypophyseal opening) characterizing jawed vertebrates. This latter change, seen in the Galeaspida among jawless vertebrates, allowed the migration of tissues that would form the anterior parts of the braincase and jaws, previously blocked by the nasohypophyseal opening in jawless vertebrates such as the lamprey and Osteostraci (Gai et al. 2011; Gai and Zhu 2012).

Also, a novel theory for a heterochronic mechanism of jaw evolution, using fossil data together with developmental data, proposed that inductive mechanisms for making dermal bone were recruited from the region below the eye. These ideas were different because they emphasized the phylogenetic origin of the bones of the jaws (those that surround the cartilage supports), together with a developmental mechanism that may have been recruited to make these bones (Long et al. 2010). Long et al. (2010) proposed that because sclerotic bones (surrounding the eyes) appear in fossil species before bones of the jaw and are present in both the jawless group Osteostraci and in extant jawed forms, they are potential candidates to develop bone in the lower jaw. This is justified by developmental data in the chick showing that scleral mesenchyme can be invoked to produce bone by mandibular epithelium. Long et al. (2010) propose that this shared developmental process is co-opted from scleral bone development in jawless osteostracans to jawed vertebrates, to make bone in the jaw apparatus.

Classic and Novel Theories of Tooth Evolution

Canonical (Reif 1982) and more recent hypotheses (Smith and Coates 1998) of tooth origins have come to be known as "outside to inside" (i.e., dermal scales/denticles, located outside the mouth, in the skin, evolving into teeth along the jaws inside the mouth) as opposed to "inside to outside"; our preferred phrase is "teeth from the inside" (i.e., gill arch [pharyngeal] denticles evolving into teeth along the jaws in the mouth; fig. 1.2B, C). However, these gill arch denticles never extend outside to give rise to skin denticles (restricted instead to the internal arches), but "outside to inside" and "inside to outside" have been a convenient, if inaccurate, shorthand for "teeth only from the inside." These hypotheses have provoked much debate and a search for new and more accurate data (molecular, palaeontological) to test both. As we emphasize, W.–E. Reif (1982), a pioneer in the study of the evolutionary origins of teeth and dentitions, recognized that both the outer dermal system of skin denticles, or scales, and the inner one of oral teeth represent separate developmental and evolutionary systems. Later, Smith and Hall (1993) proposed a developmental model for the evolution of the dermal skeleton independent of teeth, although strongly linked with neural crest in both processes, as a vertebrate skeletogenic innovation (Hall and Gillis 2013).

Current Hypotheses

In the canonical theory of origins of teeth making a dentition (Hertwig 1874; "outside to inside," Smith and Coates 1998), skin denticles, or placoid scales, were utilized for dentitions once jaws evolved, when the ability to make odontodes (see box 1.1) was transferred from the external skin of the body to the edge of the jaws and into the mouth (Ørvig 1967; Peyer 1968; Kemp 1999). This theory was largely based on the observation that the skeleton of the earliest, jawless vertebrates was only external, comprised of extensive shields of dermal bone (macromeric), but also scales (figs. 1.2B, 1.5A). Tubercles (odontodes) covered the entire surface of the bone, made of dentine with a tissue structure comparable to that of dentine in the human tooth (fig. 1.5B). Other external skeletons were composed of dentine as separate denticles (placoid scales) but not joined by bone, as in the Chondrichthyes (figs. 1.2B, C, 1.5E–G) and Thelodonti (figs. 1.2B, 1.5C, D; micromeric). A challenge to this classic theory occurred when similar denticles were recognized, for the first time in a whole body fossil, and located inside the oropharyngeal cavity in the fossil jawless vertebrate group Thelodonti (figs. 1.5C, 1.6A–E; Van der Bruggen and Janvier 1993). As well, there was a realization that the pharyngeal covering of denticles was considerably more extensive in extant jawed vertebrates, in both chondrichthyan and osteichthyan fish than conventionally thought, comparable to the external scale covering. Moreover, in some taxa these were organized into distinct rows on the gill arches (Nelson 1970).

Like sharks, thelodonts had a dermal skeleton composed of separate denticles (see size of these relative to internal denticles in fig. 1.5C), but more importantly, the internal oropharyngeal denticles were organized into small whorls (fig. 1.6A, B, D, E, cf. to a shark tooth family, figs. 1.3A, C, D, 1.4A, B, and 1.6 F), but assumed to be located on the (unpreserved) gill supports (fig. 1.2B). This new data suggested an alternative to the "outside to inside" evolutionary scenario, one in which these pharyngeal denticle sets (and the developmental controls regulating their patterning into whorls and spatial, temporal organization, situated on the gill arches) were co-opted to make tooth sets. These were first in the pharynx (deep inside the pharynx at the oesophageal-pharyngeal junction), but denticle set structure and their developmental controls were then co-opted to the jaw margin. This internal skeleton of thelodonts (figs. 1.2B, 1.6A–E) was unknown at the time the original "outside to inside" hypothesis had been developed, so the novel "inside to outside" theory was proposed (Smith and Coates 1998). Thelodont scales and denticles are made of tubular dentine and assumed to form in the same way as all dentine-based structures (fig. 1.5 B–D).

Current Debate

Both the "outside to inside" and "inside to outside" theories have been vigorously contested (as discussed in Blais et al. 2011; Rücklin et al. 2012; and Murdock et al. 2013). Amendments to these theories have included the recently proposed "modified outside to inside" (Huysseune et al. 2009, 2010) and "both inside and outside" theories (Fraser et al. 2010; Ohazama et al. 2010). With respect to the latter, an odontode (in the form of a denticle or tooth) could develop wherever the relevant genes, competent epithelium (ectoderm, endoderm, or a combination; Soukup et al. 2008, as demonstrated in the salamander), and neural crest-derived mesenchyme were combined. An important point made by the "both inside and outside" theory is that this combination could occur either internally or externally (Fraser et al. 2010). In other words, odontodes and teeth are homologous units at the morphogenetic level, and a building block of all dentitions, a long accepted fact (Schaeffer 1975). From this standpoint, we again stress that the relevant question involves the origins of developmental patterning of teeth and their spatial organization in the jawed vertebrate dentition, rather than just the origin of odontodes themselves. For example, Fraser and Smith (2011) (Fraser 2011) demonstrated that spatial initiation of new denticles (scales) in the external skin of the catshark is very different from that of teeth on the jaws (fig. 1.5E–G). This implies that the skin denticles lacked any comparable developmental patterning mechanisms that could have been co-opted to form the sets of teeth in the dentition. This topic is also discussed with respect to a molecular model for genetic pattern information in dentitions versus skin-derived structures (see below; also Smith and Johanson 2012).


Excerpted from Great Transformations in Vertebrate Evolution by Kenneth P. Dial, Neil Shubin, Elizabeth L. Brainerd. Copyright © 2015 The University of Chicago. Excerpted by permission of The University of Chicago Press.
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Table of Contents


Part I Origins and Transformations

1 Origin of the Vertebrate Dentition: Teeth Transform Jaws into a Biting Force
Moya Meredith Smith and Zerina Johanson
2 Flexible Fins and Fin Rays as Key Transformations in Ray-Finned Fishes
George V. Lauder
3 Major Transformations in Vertebrate Breathing Mechanisms
Elizabeth L. Brainerd
4 Origin of the Tetrapod Neck and Shoulder
Neil Shubin, Edward B. Daeschler, and Farish A. Jenkins Jr.
5 Origin of the Turtle Body Plan
Ann Campbell Burke
6 Anatomical Transformations and Respiratory Innovations of the Archosaur Trunk
Leon Claessens
7 Evolution of Hind Limb Posture in Triassic Archosauriforms
Corwin Sullivan
8 Fossils, Trackways, and Transitions in Locomotion: A Case Study of Dimetrodon
James A. Hopson
9 Respiratory Turbinates and the Evolution of Endothermy
in Mammals and Birds
Tomasz Owerkowicz, Catherine Musinsky, Kevin M. Middleton, and A. W. Crompton
10 Origin of the Mammalian Shoulder
Zhe-Xi Luo
11 Evolution of the Mammalian Nose
A.W. Crompton, Catherine Musinsky, and Tomasz Owerkowicz
12 Placental Evolution in Therian Mammals
Kathleen K. Smith
13 Going from Small to Large: Mechanical Implications of Body Size Diversity in Terrestrial Mammals
Andrew A. Biewener
14 Evolution of Whales from Land to Sea
Philip D. Gingerich
15 Major Transformations in the Evolution of Primate Locomotion
John G. Fleagle and Daniel E. Lieberman

Part II Perspectives and Approaches

16 Ontogenetic and Evolutionary Transformations: Ecological Significance of Rudimentary Structures
Kenneth P. Dial, Ashley M. Heers, and Terry R. Dial
17 Skeletons in Motion: An Animator’s Perspective on Vertebrate Evolution
Stephen M. Gatesy and David B. Baier
18 Developmental Mechanisms of Morphological Transitions: Examples from Archosaurian Evolution
Arhat Abzhanov
19 Microevolution and the Genetic Basis of Vertebrate Diversity: Examples from Teleost Fishes
Sydney A. Stringham and Michael D. Shapiro
20 The Age of Transformation: The Triassic Period and the Rise of Today's Land Vertebrate Fauna
Kevin Padian and Hans-Dieter Sues
21 How Do Homoplasies Arise? Origin and Maintenance of Reproductive Modes in Amphibians
Marvalee H. Wake
22 Rampant Homoplasy in Complex Characters: Repetitive Convergent Evolution of Amphibian Feeding Structures
David B. Wake, David C. Blackburn, and R. Eric Lombard


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