TABLE OF CONTENTS

ABSTRACT………………………………………………………………………………..………2

INTRODUCTION …………………………………………………………………………………. 3

WHAT IS COMPLEXITY? ………………………………………………………………... 3

HIERARCHY ……………………………………………………………………………... 5

DIVISION OF LABOR & PARTS …………………………………………………………...7

COMPLEXITY VERSUS REDUNDANCY…………………………………………………… 8

REFINED DEFINITION OF COMPLEXITY ………………………………………………… 9

WHY FOCUS ON WHALES?..... …………………………………...... …………………..…9

METHODS………………………………………………………………………………..………14

APPLICATIONS …………………………………………………………………………. 20

SOURCES OF DATA ……………………………………………………………………... 20

RESULTS ………………………………………………………………………………..………..20

DISCUSSION….………………………………………………………………………………..… 28

TREND TOWARDS SIMPLICITY ...………………………………………………………...28

FEEDING BEHAVIOR OF EXTINCT CETACEANS ……………………………………..….. 30

ROLE OF HABITAT IN DENTITION SIMPLIFICATION ……………………………………. 31

CONCLUSIONS …………………………………………………………………………………...35

ACKNOWLEDGEMENTS ………………………………………………………………..………. .36

APPENDIX A……………………………………………………………………………..……… 37

APPENDIX B……………………………………………………………………………..……… 39

APPENDIX C……………………………………………………………………………..……… 40

REFERENCES……………………………………………………………………………………. 42

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ABSTRACT Over billions of years, evolution has given rise to organisms that have increased dramatically in complexity, from microbes alone to communities that include modern humans and the great whales. But change in individual lineages, occurring by chance and in adaptation to unpredictable circumstances, does not necessarily involve increasing complexity. Complexity may increase or decrease depending on the immediate situation. Metrics of change based on a single unit, such as numbers of genes or cells, are inadequate to quantify such shifts in complexity, because the structures of organisms and communities are hierarchical. Teeth and jaws of cetaceans provide an opportunity to assess changes in complexity simultaneously at different levels of organization. A set of 17 standardized variables has been established to characterize the form of each tooth in the cetacean jaw. These include aspects of shape, curvature, carinae, serrations, cusps, and other attributes that vary according to the degree of morphological differentiation within the jaw and among taxa. Measures of complexity for each tooth in the jaw are derived from these variables. These indices of the complexity of individual teeth are integrated to derive simple information functions that quantify the complexity of the dentition as a whole. Our preliminary data show that the earliest cetaceans, derived from terrestrial, hoofed mammals, had fairly simple teeth, with a modest degree of differentiation in the jaw. By Oligocene time, taxa with more complex teeth had emerged, but dentitions did not become significantly more differentiated. Subsequently, the trend changed. Tooth forms in most lineages became simpler and much less differentiated, most dramatically among the mysticetes, where teeth were lost and replaced by baleen. These paths of change at two levels of organization represent a common pattern of evolution. A novel structure emerges, it is replicated to constitute a series of elements, and these evolve more or less independently to take on varied functions. Finally, the entire structure is refined as a single, highly integrated functional system, or it is lost as further novelty emerges, typically at a higher level of organization.

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INTRODUCTION

The transformation of cetaceans from scavenging terrestrial carnivores to streamlined oceanic hunters and suspension feeders within about 30 million years provides an excellent opportunity to clarify our understanding of patterns of evolutionary change in complexity. In spite of extensive discussion of the evolution of complexity, there is no one metric by means of which to assess such change. This is a result of difficulty in defining parts that remain comparable in complex structures with multiple hierarchical components. Here we define metrics that can be used to assess change in complexity at two hierarchical levels, in individual teeth and in the set of teeth that constitutes a cetacean jaw. Our data enables us to assess change in complexity simultaneously at two different levels of structural organization, thereby enhancing our understanding of the major patterns of cetacean evolution.

WHAT IS COMPLEXITY? Complexity is widely acknowledged as an important general property of natural and artificial systems, but it has no single definition. The idea itself is so widely used in everyday expression that people tend to take it for granted, assuming that structural complexity manifests itself simply as something with many intricate parts. We recognize systems with many parts, many different kinds of parts, and a great variety of connections amongst those parts as being complex. Groups of parts with a common structure or function that can consistently be recognized among the organisms under study constitute levels of organization at which complexity can be compared. Further, in systems like living organisms and human activities, a distinction can be drawn between structure and dynamics, which is to say between complexity of form and complexity of interaction (McShea 1996). There is also a subtle relationship between complexity and order that needs to be clearly understood. In some systems, for some purposes, it is appropriate to identify complexity with disorder, which allows for more possible states. In living systems, however, maintenance of complex structure and function depends upon the highly ordered integration of similar and different components. Given a wide array of definitions based on various aspects of complexity, it is increasingly evident that the concept itself is very hard to pin down. Most people have a solid grasp on what complexity is. Scratch below the surface, however, and one finds that different observers have strikingly different comprehensions of the concept.

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All too often, the preconceived notion that evolutionary change goes hand-in-hand with increased morphological complexity is taken for granted, as such a trend seems “too obvious to question” (McShea 1996). In the long run, as a net effect, this holds true. If one traces the evolution of life on Earth over its entire span, organisms are seen to have been transformed from primitive microbes into creatures such as sperm whales, marking an obvious transition from simple to complex anatomy. This has been expressed in more abstract terms, with the suggestion that “In evolution, it is clear that the hierarchical maximum—the degree of nestedness of the hierarchically deepest organism in existence—has increased over time.” (Marcot & McShea 2007). Moreover, an irreversible relationship between morphological complexity and evolutionary change over time is evident. Complexity is likely to increase, on the average, as certain evolutionary advances can be compared to bridges that, once crossed, cannot be retraced. This is one aspect of Dollo‟s Law, which states that the same species or organic structure cannot appear twice in evolutionary history, and thus evolution is not reversible. For example, “No solitary bacterium has ever arisen from a eukaryotic cell” (Marcot & McShea 2007).

More empirical arguments suggest that evolutionary complexity is driven in large part by natural selection. According to Bonner (1988), selection favors increasing complexity because complex organisms are composed of more specialized components, and thus their internal division of labor is much greater. As expected, with increased division of labor comes improved effectiveness of the working parts, enabling the organism to adapt to novel situations (Bonner 1988, McShea 1993). Further, Bonner argued that the emergence of higher-level individuals is evolutionarily favored for their large size. Size increase allows division of labor and thus differentiation among lower-level entities. Logic dictates that selection should favor collaborations among groups of lower-level entities, leading to increased interaction and complexity (McShea 2001b).

If a larger organism has more working parts, does it necessarily mean that bigger is better? Are larger organisms more complex than smaller ones solely on account of increased size and division of labor? Would a more specialized animal lacking the varied skill set of its generalist peers be considered simpler? Not necessarily. We will see here that certain organisms have become adapted to circumstances where smaller and more specialized (thus simpler as

[4] defined above) components are most effective. Larger organisms tend to be more complex simply by virtue of being larger. Structurally simple organisms may evolve to large sizes, especially in the case of colonies, but generally scaling factors require that they be more complex. While there is general acknowledgement that evolutionary complexity has progressively increased, it is not the case that this necessarily occurs in any given clade, at the level of evolution of particular genera, families or even higher taxa.

HIERARCHY While it may be relatively easy to define complexity in broad terms, it is very difficult to quantify complexity for an entire organism. Body size and genome size have been employed as proxies of complexity as reviewed by Bonner (1988), but these standing alone have a relatively low correlation to overall complexity. At lower taxonomic levels, most previous studies of morphological complexity employ metrics that quantify it at a single hierarchical level of structure. In the simplest terms, structural components on the same hierarchical plane can be thought of as an assemblage of similar parts. In the cells of our own bodies, the nucleus, ribosomes, and mitochondria are distinct components. These cell parts can exist on the same rung of the hierarchical ladder. Join these components together and we recognize a basic building block of higher organisms, the eukaryotic cell. This constitutes the next rung on the ladder. An ensemble of these cells, working together to carry out a specific task, forms a tissue, which can be said to be another rung. Tissues join to make up organs, which work together as organ systems, the key functional components of individual organisms. Each of these hierarchical levels is a distinct rung on the ladder, and each calls for a unique metric if organisms are to be compared in terms of their complexity. However, these comparisons, effective only for assessing the complexity of a single rung of the ladder, have a limited bearing on overall complexity.

Further, Marcot and McShea (2007) define complexity in terms of three properties and their hierarchical relationships: connectedness, differentiation, and intermediate level parts. Connectedness refers to the (apparently) greater degree of integration among parts. Differentiation alludes to the greater degree of disparity among parts or part types. Finally, intermediate level parts refers to the interpolation of intermediate hierarchical structures (tissues

[5] and organs) between the lower and upper levels, as between the cell and the entire organism (McShea 1993). This notion of hierarchical structure is an aspect of complexity that “in turn is often understood in a broad sense as a kind of summary term for organismal features associated with adaptedness, sophistication, intelligence, or progress generally” (McShea 2001a).

A system is organized hierarchically if, as defined by H.A. Simon, it is “composed of interrelated subsystems, each of the latter being, in turn, hierarchic in structure until we reach some lowest level of elementary subsystem.” (Simon 1962). Hierarchical complexity is illustrated well by Simon‟s analogy of drawing a face. He urges the reader to start “with the most obvious of characters—first outlining the face then adding ears, eyes, nose, mouth, and hair before moving to lips, teeth, pupils, and eyelashes until the limit of one‟s knowledge of anatomy is reached.” (Simon 1962). In such a way, the reader breaks down the face into a number of levels, getting more and more specific with each successive stage until all recognized attributes of the face have been added. Comparisons, however, cannot be made across hierarchical levels. Types of faces can be compared with one another, as can types of noses or eyebrows, but components defined at different hierarchical levels cannot be quantified in the same terms. Thus, a distinction between vertical and horizontal complexity emerges to help further explain the notion of hierarchical complexity.

The face exercise depends on recognition of a vertical hierarchy, defined here as vertical complexity. Each higher level contains all the entities at levels below it, and includes them as parts. This stands in contrast with the idea of a horizontal complexity, in which the number of types of parts at a given level are assessed, for example as types of cells, eyebrows, noses, or teeth (McShea 2001). In the case of teeth, for example, an analysis of horizontal complexity might be based on numbers of molars, premolars, canines, and incisors.

To analyze the complexity of an object, one must either restrict the study to a single horizontal level of complexity or develop a set of criteria that can be applied on all levels, across the hierarchical spectrum, something which is not easily done. The vertical, hierarchical complexity of skeletal elements of a whale includes the microstructual elements of the teeth, which in turn comprise their enamel, from which teeth within the jaw are in part made. Teeth

[6] aligned together form the jaw, which is attached to the skull. Finally, the skull caps off the anterior end of the skeleton. Other elements of the cetacean‟s skeleton stand in logically similar relations to the structure of the skeleton as a whole. Analysis of structures at adjacent hierarchical levels provides a better understanding of the overall complexity of the organism. Comparison of cetacean teeth individually shows change in the level of sophistication of different types of teeth across evolutionary time. Comparison of teeth to tooth sets adds a whole additional dimension to the puzzle. In this study, I will analyze the two components, one a subset of the other, to assess the overall complexity of cetacean jaws, which bear in turn on their diets, behavior, and patterns of evolution.

Jaws are composed of bone, muscle, and a wide array of different types of teeth which themselves have a multitude of composite parts. The definitions of parts may differ on distinct hierarchical levels, and for that reason parts such as a tooth must be characterized using a metric different from those applied to objects on different hierarchical levels, such as jaws. When considering how complex a form may be, it is important to consider how many parts make up the object in question, how many of each kind there are, and how these parts are integrated, interacting with their neighbors across hierarchical levels. Complexity of form is hierarchically entwined with function, which in turn relates to the ecological roles of the organism in the community and its working parts.

DIVISION OF LABOR & PARTS Linking structure and function, Simon (1962) emphasized division of labor as a source of increasing complexity in evolving biological and social systems. Simply put, the more division of labor that takes place, the more complex a system becomes. This can be seen in the social structure of an ant colony, where in contrast to a solitary ant, forced to forage, reproduce and fight for itself, a colony divides its labor among a variety of specialties. While individuals in the colony lack the generalist capabilities of the solitary ant, they make up for this by being part of a multifaceted hierarchy, each specialist honing a single skill (Anderson and McShea 2001). Thus, the colony as a whole proves more complex than an equivalent number of solitary ants.

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McShea (2002) points out that division of labor in an ant colony (or in our case that which took place during the course of evolution from an early ancestral whale with a heterogeneous jaw to the much more homogenous jaw of a porpoise) involves a “transfer of complexity.” In the case of tissues, cells lose parts internally as they become parts at a higher level within the multicellular entity. Thus tissues, organs, and more cell-to-cell collaborations emerge. “In the history of life, as organisms combined to form higher-level functional entities, functional demands on these organisms would have been reduced.” (McShea & Venit 2001). A reduction in functional demands on the entity in question is accompanied by a reduction of part types it contains. Selection tends to favor a loss of part types in the interest of economy (McShea & Venit 2001). In dolphins, this is expressed by simplification of ancestral tooth types which are reduced to a single form of peg-shaped tooth in return for a higher degree of specialization within a particular niche. Delphinids are effective predators, despite having what will be shown here to be some of the simplest types of teeth. This can be explained in terms of the fundamental idea of cellular loss for multicellular gain. Here, in the case of dolphins, there is a loss in structural diversity of the jaw for a gain in functional behavior.

COMPLEXITY VERSUS REDUNDANCY Finally, one must be careful to differentiate between what appears complex and what is, in reality, simple redundancy. Things can appear complex on account of the frequency of repetition of their parts, which may be based on repeated expression of the same elements of the genetic code. “How complex or simple a structure is depends critically upon the way in which we describe it. Most of the complex structures found in the world are enormously redundant, and we can use this redundancy to simplify their description.” (Simon 1962, p. 215). In his study of the complexity of a series of limbs in living and extinct arthropods, Cisne (1974) observed that branchiopod crustaceans with more than 50 pairs of limbs are “phyletically not the most primitive, but rather are specialized in this one respect. The presence of so many limb pairs of the same type lowers the information content per pair.” (Cisne 1974, p. 348). In this study, we show that the dentitions of dolphins and porpoises, which are by no means primitive, have dentitions that are likewise of low horizontal complexity. Here, there is a trade off between decreased jaw complexity and increased behavioral complexity.

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REFINED DEFINITION OF COMPLEXITY Morphological complexity, as defined in this study, depends on the number of multiple hierarchically organized parts that are interconnected and interact in many ways, constituting structures with more of less differentiated functions that allow a division of labor. This definition rests on the supposition that the morphological complexity of a structure or organism can be characterized by the number of elements of which it consists (McShea 1996). This definition, and the methods described below render complexity empirically tractable. However, it is important to note that this analysis focuses on a single aspect of the cetacean, its jaws, and thus does not entirely reflect change in the complexity of the organism as a whole.

WHY FOCUS ON WHALES? We seek to assess evolutionary change in complexity in a system where we can observe and measure change on more than one level of hierarchical organization. By this means, we expect to gain a clearer understanding of patterns of change in complexity over time than can be obtained using any single metric. We chose to study the transformation of cetacean teeth and jaws, as cetaceans evolved from scavenging terrestrial carnivores to streamlined oceanic hunters and suspension feeders. Using a few basic equations, we will quantify the complexity of both individual teeth and whole jaw sets. Teeth and jaws are well preserved in the fossil record, and mammalian dentitions can be indicative of age, diet, habitat, and even the health of the organism. Consequently, this system is a rich source of information on cetacean evolution and trends in the evolutionary complexity of cetaceans through time.

In the Origin of Species, Darwin (1859) imagined an evolutionary transition that would not be adequately documented for another 120 years. He could “see no difficulty in a race of bears being rendered, by natural selection, more and more aquatic in their structure and habits, with larger and larger mouths, till a creature was produced as monstrous as a whale” (p. 202). In due course it would be shown that Darwin was not far off in his speculation. Over the past 30 years, it has been established that cetaceans evolved from semi-aquatic forms like Pakicetus—a wolf-sized, possibly hoofed mammal that skulked on riverbanks—through a series of increasingly aquatic predators that ultimately gave rise to both the odontocetes, or toothed whales, and the toothless mysticetes, the baleen whales.

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For an odontocete, teeth are the tools of its trade. Variation in tooth form expresses the nature of these cetaceans‟ ecological impact, thus helping to define their specialization. As a group of animals evolved from ancestors with a very different mode of life, their teeth might be expected to have acquired increasingly specialized structures to serve their new purposes. Our objective here is to assess the patterns of change in tooth form and variety that were involved in the cetacean transition from land to sea.

Rewind the clock back 50 million years to the early Eocene. The warm Tethys Sea had not yet retreated from what are now the arid lands of modern Pakistan. Shallow seas extended over large swathes of western Asia and the Middle East. This ocean teemed with life, but since the extinction of plesiosaurs and mosasaurs at the end of the Cretaceous, it had remained devoid of large reptilian predators. Eventually a carnivore of modest proportion, wolf-like save for its hooves, extended its hunting from the land into rivers. This pioneer and its relatives gave rise to the archaeocetes, which evolved rapidly to become fully aquatic within 10 million years (Uhen 2010). As the archaeocetes migrated from rivers and deltas to bays and eventually the oceans, these ancestral whales became increasingly streamlined, losing limbs and simplifying their dentitions as they adapted in order to exploit new kinds of readily available prey.

The earliest relatively well-known cetacean, based initially on a small, incomplete skull similar in size to that of a coyote, with associated fragmentary teeth, was discovered in western Pakistan (Gingerich and Russell 1981). The skull fragments of this Pakicetus (Figure 1a) and the sediment in which these fossils occur suggest that the animal lived along shallow river channels, foraging to find everything from small fish to crustaceans, and living at least part of its life in the water (Williams 1998). Pakicetus was remarkably canine, with well developed molar, canine and incisor teeth. Initially treated as a mesonychid, Pakicetus threw up a few red flags when it was discovered that its molar teeth displayed large accessory cusps— a feature found only in whales (Thewissen et al. 2001). Middle ear bones with auditory structures similar to those of cetaceans affirmed its status as an ancestral whale.

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Ambulocetus natans (Figure 1b) was also discovered in the foothills of the Himalayas, in rocks about two million years younger that suggest a different depositional environment—that of a marine swamp (Thewissen et al. 1996). It appears that Ambulocetus, unlike its ancestor, was now primarily aquatic, living in bays and estuaries. About three meters long and resembling a furry crocodile, Ambulocetus had reduced the long, thin legs of Pakicetus to much shorter and sturdier ones (Thewissen & Williams 2002). Probably too unwieldy to be very quick in the chase, Ambulocetus was probably an ambush predator like crocodiles (Perrin, Wursig and Thewissen 2008).

FIGURE 1: Pakicetus and Ambulocetus reconstructions, by natural history artist Carl Buell.

FIGURE 2: The overturned skull of Maiacetus inuus (a close contemporary of Ambulocetus) in false color, showing components of skull bones (grey) and teeth (brown), among other morphological features. From Gingerich et al. (2009).

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By about 40 million years ago, the fully-aquatic basilosaurids were far more like modern whales. Flippers had replaced toes, a relatively streamlined body had replaced the stout frame of Ambulocetus, and they had evolved to reach an average adult length of five meters, the typical proportion of modern whales. However, they still retained the articulated limbs of their ancestors (Thewissen and Williams 2002). The remarkable Basilosaurus, snake-like in form and growing to 16 meters long, was a fearsome predator. Unlike modern odontocetes, the basilosaurids retained several types of teeth from their pakicetid ancestors, ranging from long curved canines and incisors to triangular, serrated molars (Owen 1841, Thewissen and Williams 2002).

By the middle Oligocene, the heterodont dentitions of earlier cetaceans had largely been replaced in odontocetes by much more uniform rows of teeth, generally more numerous and often homodont, with the single roots and conical crowns that are typical of modern cetaceans (Figure 3).

FIGURE 3: A short-beaked common dolphin (Delphinus delphis), showing rows of repetitive, near-identical conical teeth. From the collection of the Tullie House Museum and Art Gallery (http://www.skullsite.co.uk/Whale/whale.htm)

A number of environmental factors may have prompted the rapid evolutionary radiation of the cetaceans. The initial shift from land to aquatic settings came soon after an abnormal fluctuation in climate, around 55 million years ago, a heat wave known as the Paleocene-Eocene Thermal Maximum, or PETM (Figure 4). The earliest archaeocetes such as Pakicetus may have developed during this time to fill the recently-emptied ecological niche, allowing them to thrive and develop with little competition. The PETM can be interpreted from a major excursion in δ18O in shells of benthic foraminifera, indicative of a huge deviation in ocean temperatures at this time. There is much debate over the cause of the event. However, there is an interesting correlation between the subsequent more gradual rise in temperature and the burst of archaeocete

[12] speciation. During this interval, the ocean chemistry was dramatically altered, leading to rapid change in the environment, and thus a chain reaction in swift speciation (Zachos et al. 2001; Woodburne et al. 2009, Clementz et al. 2011).

18 FIGURE 4: Fluctuating benthic levels of δ O in the ocean over the past 65 million years. The red line is an indication of the height of archaeocete speciation (Taber 2011).

The rapid experimental transformation of cetaceans, in which new forms repeatedly emerged and soon left the stage, proves ideal for a study of change in complexity. The adaptation of their dentitions in particular reveals a transition from a diversified set of teeth used to cut, grind, and chew to—in the most extreme cases—sets of nearly identical peg-like teeth used to capture prey and gulp it down whole or in chunks.

The goal of this study is to explain the apparent discrepancy between relatively short- term changes in complexity like those that have occurred in the course of cetacean evolution, and the long-term increase in complexity that has occurred over the entire history of life on Earth. Our data reveals a well-defined trend from complex heterodonty in the earliest, land-dwelling ancestors of whales to simplified homodonty among the modern odontocetes. By the dawn of the Oligocene, a mere sixteen million years after the earliest archaeocete put hoof to water, the earliest forms of modern cetaceans, with a whole new range of tooth forms and jaws, had emerged. Hence, the cetaceans provide an ideal case study, by means of which to reassess long- standing and more recent perceptions of the evolution of complexity.

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METHODS Most attempts to quantify evolutionary trends in complexity have focused on units at one level of organization, such as number of cell types (Bonner 1988), the disparity of arthropod limbs (Cisne 1974), or proportions of vertebrae or centipede segments (McShea 1993; Fusco and Minelli 2000). The interpretation of such analyses is sometimes confounded by the fact that the structures of living organisms are hierarchical (Salthe 1985; McShea 1996, 2001a), with varying degrees of complexity at and across different levels of organization. Here, we seek to define evolutionary complexity in such a way that it can be consistently measured simultaneously at more than one level in order to explore interactions between levels of organization.

We set out to answer two main questions. Initially, we sought to define morphological complexity in a way such that it can be consistently measured at more than one hierarchical level of organization. Beyond this, we wanted to apply our methods to determine whether patterns of cetacean evolution substantiate or depart from the common notion that evolutionary change begets increasing complexity. Complexity is an important general property of natural and artificial systems, but it has no single definition. As laid out above, we recognize that complex systems are comprised of many parts, many different kinds of parts, and a variety of connections amongst those parts. Further, we recognize that in living systems, maintenance of complex structure and function depends upon the highly ordered integration of similar and different components.

The working parts of an organism and its structure as a whole are hierarchically linked to function, which is in turn indicative of the organism‟s ecological roles in the community (Bock and von Wahlert 1965). To determine the complexity of an object within a hierarchical level, we needed to establish metrics that can be applied to the forms of both teeth and jaws. To characterize the forms of individual teeth, we have established a tooth “morphospace” (Figure 5). This design space embraces all the simple and more specialized features of cetacean teeth of which we are aware. Then, having determined individual tooth complexity, we can assess the assemblage of teeth, along the jaw length, to determine the complexity of the jaw as a whole. These data can be used to track the evolution of cetacean tooth and jaw complexity through time.

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FIGURE 5: Tooth Morphospace. Each tooth is characterized in terms of the shape of its cross-section (S0, S1, S2), tooth height (H0, H1, H2), number of facets (F0, F1, F2), tooth apex shape (A0, A1, A2, A3, A4), curvature (C0, C1, C2, C3, C4, C5, C6, C7, C8, C9), lateral tooth splay (L0, L1, L2), anterior or posterior splay (M0, M1, M2), change in size from the previous tooth (Z0, Z1), carinae present (R1, R2), type of cusps (P0, P1, P2, P3), denticles present (D1, D2), serrations present (X1, X2, X3), striations present (T), grooves present (G), neck/bulb present (N), barbs present (B), hooks present (K), and left-right asymmetry of expression on two sides of the jaw (Y).

We measure the complexity of individual cetacean teeth in terms of the number of specialized features they exhibit. Eighteen variables, with varying numbers—from 1 to 10—of possible states are defined in the morphospace. Complete cetacean jaws were examined to arrive at a descriptive formula for each tooth. The basic, „ground state‟ for a cetacean tooth is an erect cone of average height, with a circular cross-section and no curvature or other specialized features. This simple form, represented as S0H0F0A0C0L0M0Z0, may be modified by the presence of specialized character states such as its curvature, orientation in the jaw, presence of carinae (cutting edges), serrations, cusps, striations and other features (Figure 5). Hence, a tooth is characterized by a formula consisting of one state in each of eight categories of shape and

[15] orientation, plus any of ten additional types of distinctive features that may be present. In terms of this model, a human molar has the formula S1H0F1A3C0L0M0Z0P2 and an incisor is

S1H0F1A4C0L0M0Z0. The resulting data are ideographic and semi-quantitative in nature.

These data (see Appendix B for sample raw data and compilation) provide two measures of the complexity of individual teeth. One is simply the number of characters expressed by a tooth beyond the ground state, defined above. This is the number of “parts” (McShea 1996, p. 479). The other measure is the sum of scores, where characters are assigned values 1, 2 or 3 according to the complexity of the sort of mathematical function that would be required to define the feature. In our data set, the latter metric yields results little different from the number of characters, to which we confine our analysis here.

It is more difficult to define and measure the complexity of a set of teeth, where each tooth may differ in one of more of several variables. McShea (1991), setting out to differentiate and assess evolutionary complexity, observed that “it is sometimes worthwhile to document the obvious.” He correctly realized the difficulty in quantifying such an abstract concept. In an analysis of change in the patterns of repetition of six separate measurements of mammal vertebrae, McShea (1992, 1993) employed three metrics to assess the deviation in design of each part from those of its neighbors. Logically, McShea supposed that the degree to which the structure of the vertebral column is either hetero- or homogenous is a measure of its overall complexity. The metrics he employed are defined in Table 1.

TABLE 1: Metrics of complexity: (I) range, (II) polarization, (III) irregularity, all from McShea (1992); (IV) sum of changes in slope of measurements relative to spacing of repeated elements, as defined by Fusco and Minelli (2000). [16]

The range (Equation I) between Xmin and Xmax represents the scope of variation in a single measured variable. As simply the difference between the highest and lowest numerical values, it is zero where all cases have the same value. It does not take the number of cases, teeth along one side of the jaw in our study, into account. Polarization (Equation II) is a measure of asymmetry in the distribution of values above and below the mean. It is independent of the number of cases, hence of spacing of observations if the variable is continuous. Irregularity (Equation III) is a function of the difference in value for each case, compared with that of its predecessor in the series, averaged over all cases. It is affected by the distribution of values along the series as well as by their immediate differences.

In a study of patterns of complexity in sequences of centipede segments, Fusco and Minelli (2000) proposed an alternative measure of irregularity (Equation IV). This metric is analogous to that used by McShea (1993), differing from it in that the measurement made on each segment is compared with those taken from both adjacent segments, not only with that from the previous segment. Fusco and Minelli (2000) showed that their metric is more sensitive to changes between adjacent segments and less sensitive to the number of segments (effectively the spacing of observations) in the set.

Each of these metrics can be applied only to one variable at a time. In his mammal study, McShea (1993) conducted six separate analyses in parallel, based on six different measurements of the vertebrae. In our study, these metrics can be used to assess jaw-level complexity in terms of changes in the number of characters expressed from tooth to tooth. However, this approach overlooks much of the richness in our data set, as it does not take the loss or gain of specific features into account. If two features are eliminated from one tooth to the next, and two different features are introduced, there is no net change in complexity of the individual teeth. But, these changes are substantial in relation to the complexity of the tooth set, and thus to that of the jaw as a whole.

Cisne (1974) sought to quantify the complexity, involving many variables, represented by change in numbers and kinds of modular units in a series. In his study of the evolution of arthropod limbs, he used a Brillouin information function:

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incorporating the numbers of pairs of limbs 'n' in each of a predetermined set of potential limb types and the total number of limbs, N. This approach is theoretically sound and it yields excellent results, but it requires that the individual modules can be assigned to a fixed set of categories. If our data had consisted of varying numbers of molars, premolars, canines and incisors, which can be recognized in the earliest cetaceans, we could have used this approach. In fact, the individual teeth of cetaceans soon evolved to adopt forms that do not correspond with these categories, which are too broadly defined and ultimately inappropriate for our purposes.

None of these methods is applicable to quantify irregularity—complexity at the level of the dentition as a whole—on the basis of our multivariate data, where one, two or more characters may change from tooth to tooth. The simplest measure of complexity of the jaw as a whole is the total number of characters expressed by all teeth in the series. A better index is one based on the ratio of the total number of characters expressed in the set to the average number of characters expressed by an individual tooth:

where Jtc is the total number of characters expressed in the tooth set, TC.ave is the average number of characters expressed by any given tooth, and Nt is the number of teeth along one side of the jaw. This index is standardized in such a way that when all teeth in the jaw are identical, Ctc = 0, and when every tooth has a unique set of specialized characters, with no overlap among teeth

(unlikely when more than one tooth is present) Ctc = 1.

The index we have just defined reflects the expression of tooth characters, but not relationships between individual teeth. To take this into account, we established a measure, termed the average shift, as the average number of characters that change from one tooth to the next. This shift is zero in a jaw where all teeth are identical and correspondingly larger where the teeth are more disparate. It varies linearly with the number of teeth in the set, all other things being equal. The latter property of this function is not ideal, just as a measure of species diversity that varied linearly with sample size would be inappropriate. This led us to conceive of an analog

[18] of the Shannon Diversity Index as a more appropriate metric of irregularity among jaws that vary substantially in numbers of teeth.

The Shannon Index is a non-linear measure of entropy, widely used in ecology as a measure of species diversity, that takes both species richness and evenness of representation of species in a sample into account. In the case of the Shannon Index, the diversity, S, is equal to the sum of products of pi times its logarithm, where pi is the frequency of a given species. In the case of our metric, complexity, C, is equal to the sum of products of ai — the shift from one tooth to the next of i = 1, 2, 3, n… characters — times pi , times its logarithm, where pi is the frequency of teeth exhibiting a shift of 'a' characters.

One limitation of this metric is that a graded series of teeth, such as those of an angler fish or the Ganges river dolphin, in which each tooth differs from its predecessor in the series to about the same degree, and a jaw in which one or a few teeth differ dramatically from others that are all similar, as in a sabre-toothed cat, may yield the same value of C. This metric provides a measure of information richness of the jaw, not a characterization of its pattern.

Graphical display of these metrics, plotted against geologic time, allows us to document ways in which the complexity of individual teeth and that of whole dentitions have changed over the entire course of cetacean evolution. Plots of measures of jaw complexity against tooth complexity enable us to explore the interaction between these variables. Taken together, these analyses provide a framework for the interpretation of tooth forms and dentitions in relation to changing functions as cetaceans increasingly forsook the shoreline and put to sea.

By compiling data for a large sample of cetacean genera, we can also establish a broad context in which to infer ways that cetaceans may have adapted to their surroundings. The contrast between the differentiated teeth of Pakicetus and the strikingly similar (homodont) teeth of Tursiops exemplify aspects of the adaptations of the toothed whales.

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APPLICATIONS Our graphical models can be used to infer the likely diets and habitats of extinct cetaceans more systematically than has been possible up to now. Let‟s say, for example, that a fossil jaw has been unearthed in Wadi Al-Hitan, the famous Valley of the Whales in Egypt. Given 1) a largely complete set of teeth for at least one side of the jaw, 2) prior knowledge of the diets and habitats of living and many fossil cetaceans that are well established, 3) a morphospace documenting the possible forms of cetacean teeth, and 4) a graphical model displaying tooth and jaw forms on which diets and habitats are mapped, it is possible to establish a hypothesis as to the likely diet and habitat of the newly discovered cetacean based upon its position in the diagram. It is important to emphasize, however, that this procedure does not establish a final ecological interpretation, but rather sets up a hypothesis to be subjected to further tests.

SOURCES OF DATA The best means of obtaining data is through direct observation of cetacean teeth and jaws. We obtained most of our data from skulls of living and fossil cetaceans, one specimen from each species in nearly all cases. Almost all the material was found in either the collections of the Smithsonian‟s National Museum of Natural History and its Museum Support Center at Suitland, Maryland, or at the Calvert Marine Museum in Solomons, Maryland. We have drawn some data from the literature, which we have also used to corroborate our observations of actual specimens and as a source of information on the biology or paleobiology of cetacean genera and species. Catalogue numbers of specimens on which our observations are based are listed in Appendix A.

RESULTS A general view of life‟s evolutionary progression leads one to expect change from simple to complex. Our results show that cetacean jaws evolved towards markedly simpler dentitions in the transition from archaeocetes to both odontocetes and mysticetes. Complexity does not necessarily march forward through time as might have been anticipated. Instead, complexity may increase or decrease at any given level of organization depending on the demands of adaptation.

Early cetaceans were conservative in the number of their teeth, which varied little over the first 15-20 million years of their evolution (Figure 6). The dramatic evolutionary radiation of

[20] the odontocetes that followed gave rise to dentitions with a wide range of numbers of teeth, from a single tooth on each side of the lower jaw in some of the beaked whales (Mesoplodon) and a spiral horn, usually only on one side of the upper jaw in the narwhal (Monodon monoceros), to more than 50 teeth in a single dentary or maxilla of the river dolphin, Pontoporia. Even greater numbers of teeth occur in some other Neogene taxa. Among the mysticetes, teeth were first retained as the baleen began to develop, and then lost altogether.

Individual teeth of the archaeocetes, however, were of moderate complexity (Figure 7), staying relatively close in form to those of their terrestrial ancestors. By the end of the Eocene, much more specialized and unusual cetaceans, by now fully aquatic, had acquired teeth with a much wider range of characters. The teeth of Basilosaurus, in particular, were much more varied and complex than those of earlier cetaceans, while teeth of Llanocetus, the earliest known mysticete, were already greatly simplified. While this study lacks data for most of the Oligocene, an interesting story emerges with the late Oligocene toothed mysticete, Janjucetus. This unusual whale had teeth similar in their specialized characters to those of Basilosaurus, but even more complex. Interestingly, following the substantial increase in number of characters expressed by teeth of the dorudontids and some radical early mysticetes, the teeth of modern neocetes reverted to a number of characters similar in range to those of terrestrial and semi-aquatic archaeocetes. However, although the numbers of characters expressed in neocete teeth are similar to those of archaeocete teeth, the characters involved are quite different. Whereas archaeocete teeth feature cusps, striations, and carinae among their specialized characters, the teeth of the odontocetes tend to express features that are linked to their position and role in the jaw, such as their curvature or tendency to splay forward or laterally, away from the line of the jaw (Figure 7).

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F IGURE 6: Two modes of evolutionary change. Archaeocetes were conservative, maintaining almost the same small number of teeth throughout Eocene and Oligocene time. Subsequently, a dramatic expansion in the range of numbers of teeth occurred during the Neogene.

Key to species: Ambulocetus sp. (Ab), Balaenoptera musculus (Bm), Basilosaurus cetoides (Bs), Cephalorhynchus eutropia (Cp), Delphinapterus leucas (Dp), Dorudon atrox (Dd), Globiocephala sp. (Gb), Hadrodelphis calvertense (Hd), Inia geoffrensis (Ng), Janjucetus hunderi (Ju), Kogia breviceps (Kb), Kogia simus (Ks), Liolithax pappus (Lx), Llanocetus dentricranatus (Lc), Maiacetus inuus (Mc), Mesoplodon europaeus (Me), Mesoplodon grayi (Mg), Mesoplodon carlhubbsi (Mh), Mesoplodon layardi (Mp), Monodon monodontidae (Mm), Mauicetus spp. (Mu), Odobenocetops peruvianus (Od), Orcinus orca (Oc), Pakicetus inachus (Pk), Phocoena spinipinnis (Ph), Physeter catodon (Py), Pontoporia blainvillei (Pb), Prosqualodon davidis (Pq), Protocetus atavus (Pct), Tursiops truncatus (coastal) (Tt), Zarhachis flagellator (Zh). For comparison: Homo sapiens (H). Archaeocetes are identified in red ( ), odontocetes in blue ( ), and toothed and toothless mysticetes in yellow ( ).

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FIGURE 7: Mean and range of complexity, based on number of characters expressed, of individual whale teeth in each jaw. This tracking of the number of characters of teeth of extinct and extant whales across time illustrates one aspect of the evolutionary radiation of cetacean teeth (and thus, species themselves) during the Cenozoic, showing an initial increase, followed by a Neogene decrease in complexity through time. Note that beyond Odobenocetops peruvianus (Od), all whale species plotted to the right are extant. For key to species, see Figure 6.

Despite the significant jump in the range of numbers of teeth, and the change in tooth characters from archaeocetes to neocetes, odontocete jaws are not particularly complex, certainly not compared to those of the archaeocetes (Figure 8). Our simplest index of jaw complexity, based on the ratio between total number of characters expressed in the jaw and the average number of characters expressed in a single tooth, reveals a great decline in overall complexity of the dentition that was clearly recognizable by the Late Eocene. This downward trend appears to have continued through to the Oligocene, an inference that needs to be tested against more data for the early and middle Oligocene. There is a big jump from high or moderate jaw complexity to a new complexity range at the start of the Miocene, by which time some odontocetes demonstrate low or zero jaw complexity (Figure 8). By then, the, jaws of the odontocetes had

[23] completed their transformation from heterodont to integrated homodont tooth sets. The moderate complexity of an orca jaw (Orcinus orca) represents the greatest degree of complexity among modern odontocete dentitions. Data for the beluga whale, Delphinapterus, are anomalous here, reflecting a limitation of this metric. Dentitions of the upper and lower jaws of this whale earn the highest and one of the lowest measures of complexity among the neocetes on this scale. This is an artifact of a pattern of variation where each of a few characters that differ among a modest total number of teeth is expressed in a different tooth.

FIGURE 8: Plot of a simple index of jaw complexity, based on a ratio of the total number of differen characters expressed in the jaw to the average number of characters expressed in a single tooth, plotted against geologic age. For key to species, see Figure 6.

Our modified Shannon Index provides a more consistent measure of the complexity of cetacean dentitions, in terms of the irregularity of expression of tooth characters along the length

[24] of the jaw (Figure 9). Plotted against the number of teeth in the jaw, it shows a pattern similar to a Poisson distribution. The greater the number of teeth, the lower their irregularity tends to be. The sharp contrast in complexity of dentitions of archaeocetes and neocetes with similar numbers of teeth, eight to ten, is clear here. However, the tail of the distribution of neocete data to the right is largely probabilistic. If a jaw has 50 teeth, its irregularity/complexity will

FIGURE 9: Complexity of cetacean teeth and dentitions, measured as a modified Shannon function, plotted in relation to the total number of teeth along one side of the jaw. Lower or upper jaw, as available. Note that related species group closely together, and that the archaeocetes consistently occupy a very different part of the range from that where the odontocetes appear. Furthermore, the number of teeth of the archaeocetes changed very little throughout their range. For key to species, see Figure 6.

[25] necessarily be low, as it is highly improbable that 50 distinct tooth functions with associated specialized characteristics (in the extreme case) could exist in a single jaw. Realistically, the complexity of jaws with numerous teeth is always likely to be minimal, as even a few teeth that differ dramatically from a large majority of teeth that are alike will not generate high irregularity.

Comparison of the complexity of the jaw as a whole with that of individual teeth (Figure 10) best documents the striking changes in dentition that occurred in the transition from the archaeocetes to their Neogene descendants. The complex dentitions, and particularly the irregularity of the jaw in the archaeocetes, reflect the presence of several types of teeth that were relatively specialized for different purposes. This stands in sharp contrast with the dentitions of odontocetes, with individual teeth of low to moderate complexity and much lower irregularity, some modern dolphins and porpoises exhibiting true homodonty. In the majority of odontocetes, the teeth are integrated to function as a whole in ways that reflect specific diets and complex behavior, especially in the capture and subjugation of prey. Odontocete teeth often repeat, and these simple repeating forms (close to the simple cone S0H0F0A0C0L0M0Z0) reflect their integration to serve a single purpose well. This representation of our data highlights the fact that the major shift in complexity from the dentitions of archaeocetes to odontocetes is a function of the change in irregularity of the jaw as a whole. In the case of the mysticetes, the complexity of individual teeth and their irregularity were of necessity both reduced, as the teeth became vestigial or were eliminated. By the late Eocene, Llanocetus, which had simple, widely spaced teeth and insertions for baleen, was already well along this path (Figure 10). The trend reaches its logical conclusion in the emergence of the toothless modern Mysticeti, which have given up teeth entirely in favor of baleen suspension feeding. This plot shows just how anomalous Janujucetus is. Llanocetus is intermediate only in the form of its dentition and not in its evolution between Janjucetus and the toothless mysticetes. Janjucetus lived ten million years after Llanocetus in the late Oligocene, by which time its contemporary, Mauicetus, was already toothless.

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FIGURE 10: Complexity of cetacean teeth and dentitions. Irregularity of the tooth row, measured here as a modified Shannon function, plotted against the average complexity of individual teeth for living and extinct whales. For key to species, see Figure 6.

These data show that in the evolution of the Cetacea, there is a major shift towards jaw simplicity and tooth integration at the expense of disparity and specialization of teeth within the jaw. Whether this trend represents true loss of complexity, as in extreme cases among parasites, or reflects a trade-off between reduced complexity of form at lower hierarchical levels of organization and increased structural and/or behavioral complexity at higher levels, remains to be discussed below.

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DISCUSSION

TREND TOWARDS SIMPLICITY The earliest members of the animal phyla are commonly simple relative to more complex forms that have emerged among their descendants. Cisne (1974) observed that successive pairs of arthropod limbs were serially replicated and then evolved separately, individually or in groups, to serve different functions. Likewise, early mammals went through an analogous process of specialization that gave rise to distinct teeth used for different purposes: molars, premolars, canines, and incisors. If cetaceans followed this pattern, one might suppose that a cetacean with differentiated teeth, and hence a more complex dentition, is more specialized than one with a set of identical, homodont teeth.

In contrast, our data set shows that cetacean dentitions became simpler, rather than more complex, over time as cetaceans evolved from land to water. Striking shifts in the patterns of cetacean dentitions occurred during the Oligocene (Figure 10). As the odontocetes diversified, the specialized morphological features that characterize their individual teeth changed from the cusps, carinae, and striations of archaeocete teeth to aspects more attuned to the position and role of the teeth in the jaw, such as their curvature and tendency to splay out at an angle away from the jaw. These features, and the strong shift toward homodonty, reducing the complexity of the dentition as a whole in essentially all odontocetes, reflect teeth that were becoming much more adapted to function as parts of a single integrated structure. The individual functions of the teeth were reduced as they became adapted to work together to function just as well, if not better, than the heterodont teeth of the archaeocete jaw—just as ants have achieved evolutionary success by giving up aspects of their individuality to collaborate in colonies.

In the more extreme case of the mysticetes, teeth have been shrugged off altogether in favor of baleen plates—flexible, comb-like sheets of keratin that are adapted to filter large quantities of krill, copepods, and small fish. Thus, according to our data set, teeth and jaws of cetaceans have evolved to become less complex as teeth have either been integrated into more specialized organ systems or replaced by entirely novel feeding organs. In the evolution of the odontocetes, individual teeth generally tend to lose their specialized features in favor of more homodont dentitions. In fact, the entire jaw as a unit

[28] becomes much less morphologically complex, as individual teeth that formerly had unique functions are simplified and integrated to perform a single task. This meets the expectation of McShea (2001a; McShea and Anderson 2005), who predicts a loss of complexity of “parts” as they are integrated into more complex structures at the next higher level in a structural hierarchy. In this case, however, both the individual teeth and the jaw as a whole, at least in terms of its dentition, become less complex. We inferred that in cetaceans, this loss of complexity of individual teeth and the dentitions of which they are components are linked to increased complexity at a yet higher level of organization, that of cetacean behavior.

Odontocetes exhibit very sophisticated behavior in tracking, capturing and subduing their prey. Our hypothesis of increased complexity at a higher level of organization is further corroborated by the recent analysis of breaking symmetry in development of the larynx of many odontocetes, including dolphins, porpoises and beaked whales, documented by McLeod et al. (2007). The observed asymmetry of the neck has been linked in the past to echolocation, but this supposed function has not been empirically tested. What is shown is a shift in the size of the anterior choanae, creating a larger food channel on the right side of the throat, an observation McLeod et al. (2007) could correlate in 13 odontocete species to an increase in maximum prey size. They infer that this adaptation allows large items of food to be gulped without chewing, which is impractical under water. Selection for the capacity to ingest large, unchewed prey provides a sufficient explanation for increased complexity represented by the asymmetry of the larynx, hyoid apparatus and other aspects of the odontocete skull that are directly linked to the form of the larynx in their development. Thus there is a trade-off, where one aspect becomes simpler while simultaneously another becomes complex. In odontocetes and mysticetes, simplification of their dentitions is coupled with increased complexity of a feature such as throat size or development of a new organ, the baleen. In each case, this shift is related to their particular feeding behavior, involving either echolocation or filter-feeding.

This trade-off is one where cetacean jaws become markedly simpler, but at the same time more specialized for a single task—capturing and eating a particular type of prey very well. One must consider the relation between specialization and complexity carefully. Some dolphins have many teeth, all similar in form and size (e.g. Pontoporia, Figure 10), constituting relatively

[29] simple dentitions. However, dolphins are by no means primitive cetaceans, notwithstanding the simplicity of their teeth and jaws (Figure 10). Their jaws exhibit a high degree of specialization to do one thing very well. Dolphins have become adapted to a certain very specialized prey niche that requires an integrated homodont dentition, eliminating the need for additional types of teeth that are now rendered less useful. Pontoporia proves to be more specialized at a higher level of organization than a pakicetid with differentiated teeth that have distinct functions. As Anderson and McShea (2005) predict, the parts of the dolphin jaw — individual teeth — exhibit reduced complexity in accord with their integration and loss of solo roles.

As dolphin and porpoise jaws evolved, these two odontocete families experienced a great divergence in the number of their similar, repetitive, simple teeth (see Figure 6). From exceedingly numerous in the phocoenids to a severely reduced number in delphinids, the number of teeth differs greatly from family to family, and even among genera, each taxon adapting its “tool set” to unique, specialized environmental and dietary habits.

This later specialization stands in contrast with the “radiation of stem Cetacea… widely recognized as an exceptional example of a group radiating into an open adaptive zone…” (Steeman et al. 2009, p. 573, citing Uhen 2008 and Gingerich et al. 2009). As noted above, the extinction of large predatory marine reptiles at the end of the Cretaceous left the window wide open for archaeocetes to make a rapid transition from land to sea. Retaining the distinctive teeth of the earliest archaeocetes—molars, premolars, canines, and incisors—increasingly aquatic cetaceans display a relatively wide range of individual tooth characters and jaw complexity, despite having a conservative number of teeth. With dentitions opposite those of the dolphins and porpoises, unlike these modern specialists, archaeocetes may be interpreted as generalists.

FEEDING BEHAVIOR OF EXTINCT CETACEANS With additional data and further refinement, the data set and analyses used here to assess patterns of change in complexity can potentially be employed for another purpose. Our graphs provide a context in which hypotheses bearing on the dietary habits of fossil cetaceans can be framed by comparison of data derived from their teeth and jaws with results displayed in Figures 6-10. Our data strongly suggest, for example, that the feeding behavior of the Miocene

[30] platanistid Zarhachis is likely to have been similar to that of the living La Plata dolphin, Pontoporia. Preliminary assessments of the dietary choices of modern and some extinct cetaceans, superimposed on the data of Figure 10, are included here as Appendix C. These graphical models can be used, as explained in the „methods‟ section of this paper, to infer the potential dietary habits of a previously unknown cetacean, represented only by its fossil jaw, providing a quantitative test of inferences based on comparative anatomy that tend to draw selectively on more limited data.

Interestingly, just as the cetaceans simplified or lost their teeth, squid—major items of prey for many whales—abandoned the shell-skeletons of their remote ancestors. Squid had made this move much earlier, in the Mesozoic, but it is notable that both groups took to reliance on their advanced behavior to survive. Among whales, this trend was driven to a large extent by major changes in feeding behavior, including the development of echolocation to facilitate nocturnal feeding on squid (Lindberg and Pyenson 2007) and great migrations to exploit new food resources made available by Neogene changes in ocean circulation (Fordyce 1980, 1989; Steeman et al. 2009) that are discussed in more detail in the next section.

ROLE OF HABITAT IN DENTITION SIMPLIFICATION The combination of factors that drove the dentitions of the odontocetes and mysticetes towards simplicity, with the baleen whales ultimately losing their teeth altogether, is quite fascinating. It appears that global environmental and geological changes initiated a chain of events that led to the evolutionary radiation of the Neoceti (now generally supposed to be monophyletic, Fordyce and de Muizon 2001), beginning some 33 million years ago during the dawn of the Oligocene.

There is a close relationship between the changing tooth adaptations of cetaceans and their evolutionary radiation into open ocean habitats as a result of the formation of the Antarctic Circumpolar Current (ACC), around the time of the Eocene-Oligocene boundary (Fordyce 1980, Steeman et al. 2009). Furthermore, there seems to emerge a relationship between evolutionary morphological change, the appearance of much expanded encephalization (brain-body size ratio), echolocation, and potentially even large body size as a result of this chain reaction.

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Effectively isolating the Antarctic continent, the establishment of the ACC was driven by movement of tectonic plates, initially opening up the Tasmanian Seaway south of Australia in the Paleocene, and completing the circuit by opening of the Drake Passage near South America at the beginning of the Oligocene. The new current that could run along this freely-opened passage brought about severe cooling of the seaway by limiting warm surface oceanic water to the Antarctic Convergence, at a distance of about 1500 km from the continent. This caused a general build up of Antarctic ice, reduction in the salinity of surface waters, and great upwelling of nutrients, brought up mainly by the Antarctic Divergence, closer to the continent (Figure 11).

FIGURE 11: Depiction of the Antarctic Divergence, driving an increased amount of nutrients from deeper water up towards the surface. From Mann and Lazier, Dynamics of Marine Ecosystems, 1996.

The establishment of the ACC is thought to have led to the generation of a massive, locally concentrated open-ocean, cold-water food resource—based on pelagic diatoms with silica skeletons at the base of the food chain—along the circumpolar current, particularly around the Drake Passage, as a result of increased levels of nitrates and dissolved silica. This pattern of high productivity is similar to those associated with significant (but less intense) upwelling along the line of the equator and with regions of intense upwelling that run parallel to the western margins of continents. Given so much productivity of phytoplankton, a whole trophic web would have emerged, with crustaceans and fish appearing to happily gobble up the abundance of the autotrophs. Naturally, it follows that fish would have attracted larger carnivores, including both odontocetes and early mysticetes (not yet without teeth) to flourish in the food-laden sea.

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This scenario is based largely on work published over many years by Fordyce (1980, 1989) and recently by Steeman et al. (2009). Marx and Uhen (2010) sought to test the hypothesis that the availability of abundant diatoms in particular has directly driven cetacean evolution. Their methodology has been criticized on account of the fact that their test depends on diatom species diversities, which are not necessarily correlated with productivity (Pyenson et al. 2010). Nonetheless, both the structure of present-day food webs in which cetaceans participate and the coincidence in timing between the emergence of the ACC and the simultaneous radiation of filter-feeding mysticetes and echolocating odontocetes leaves little doubt that these phenomena are related.

As Marx and Uhen (2010, p. 993) have observed, “What unites these two different adaptive strategies is their effectiveness in terms of mass feeding . . .” This leads us to suppose that the emergence of the ACC likewise prompted the start of whale migration as a means to take advantage of these rich, abundant trophic webs—starting with phytoplankton and diatoms—at the times of year when they are most productive. In this initial radiation of the Neoceti, as whales were leaving continental margins, actively migrating and entering a new range of oceanic habitats, there would have been a fundamental need for wholesale re-engineering of their structure, physiology and behavior.

A key aspect of the re-engineering that occurred in conjunction with the emergence of the Neoceti was the novel development of echolocation among the odontocetes as a means to track prey in the vast expanses of the open ocean. Earlier attempts to construct a molecular phylogeny of cetaceans (Milinkovitch et al. 1993, Milinkovitch 1995) seemed to suggest that echolocation had evolved independently in more than one lineage. However, the recent phylogenetic analysis of Steeman et al. (2009) supports relationships that are more consistent with those long inferred from morphology. Echolocation appears to have evolved once, close to the time of origin of the odontocetes, aiding their increasing exploitation of the open oceans and emerging opportunities presented by the development of the ACC.

Also in parallel with these developments came a rapid expansion in whales‟ brain sizes. Data of Marino et al. (2004) show a wide separation between the encephalization quotients

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(which compare brain sizes relative to a given body size) of odontocetes and archaeocetes. So, we see that remodeling of the relatively complex teeth and jaws of the archaeocetes, giving rise to highly integrated, more nearly homodont jaws of the odontocetes, occurred at the same time as the emergence of novel patterns of complex behavior. This complex behavior, underwritten by large brains and documented by anatomical evidence of echolocation, is inferred to have been employed in complex feeding behavior, including long-range migrations. Loss of structural complexity at two levels of organization in the jaw was offset by new levels of complexity in feeding behavior, including novel adaptations associated with gulping large prey.

A second period of ocean restructuring resulted from plate motions with effects of a different kind during the Miocene and Pliocene. At this time, oceanic gateways that had long kept a circum-tropical ocean (Tethys, Paratethys) open now restricted its flow, ultimately closing at both ends of the Mediterranean and at the Isthmus of Panama. Together with further steepening of the climatic gradient as ice continued intermittently to build up in Antarctica, this led to an intensification of ocean circulation (Steeman et al. 2009) and increased upwelling of nutrients along north-south continental margins. These events prompted another great radiation of dolphins, porpoises, and beaked whales, partly by vicariance, as new species emerged in newly isolated regions. However, the kinds of changes in teeth, jaws and other adaptations of cetaceans that occurred during this radiation were largely variations and refinements of established themes, unlike the radical innovations of the Oligocene.

Once established in oceanic habitats, the cetaceans evolved to adopt a range of moderate to very large sizes. The largest whales are mass feeders (Goldbogen et al. 2007; Marx and Uhen 2010), like the herbivorous sauropod dinosaurs. Large whales may have grown to their enormous sizes to achieve economies of scale in traveling great distances with relative ease, simultaneously gaining some protection by limiting their vulnerability to very few potential predators. Another reason for their massive size may result from their teeth. Both the odontocetes and mysticetes have lost the ability to predigest their food. Consequently, they are forced to expend comparatively more energy in digesting it than would an animal that breaks its food into smaller pieces. Being warm-blooded animals, whales would have likely needed to conserve this energy for digestion and thus would initially have limited their radiation to tropical environments.

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However, once the incredible rewards offered by the ACC became available, whales ventured into these colder habitats, evolving blubber and larger bodies to cope with the low temperatures.

CONCLUSIONS In this study, we sought to do two things: first to understand the abstract concept of complexity as it applies to biological form and to develop metrics by means of which it can be measured at more than one level of structural organization; and second to apply these concepts to enhance our understanding of the evolutionary history of cetaceans — or, more specifically, that of their teeth, jaws and feeding adaptations. We have shown that cetaceans exhibit a strong shift towards jaw simplicity and tooth integration at the expense of tooth and jaw variation. Complex dentitions of the archaeocetes include teeth that were relatively specialized for a variety of purposes. In contrast, odontocete dentitions, with individual teeth of low to moderate complexity, are also low in irregularity, some even homodont. Largely similar teeth are integrated to function as a whole in ways that reflect different diets and behavior, especially capture and subjugation of prey. Teeth of the odontocetes—modern toothed cetaceans with origins in the early Oligocene—are iterated and coordinated to serve one purpose well, or they are greatly reduced in number and complexity. Alternatively, their roles having been taken over by other anatomical features or new modes of feeding behavior, exemplified in the emergence of the toothless mysticetes, which have given up teeth entirely in favor of suspension feeding. Recognition of the reality of life‟s long-term evolutionary history, in the course of which complex higher organisms have emerged from simple life forms of the remote past, prompts a general expectation of change from simple to complex. The fact that cetacean jaws have evolved to accommodate markedly simpler teeth and dentitions indicates that complexity does not necessarily march forward through time. It is capable of fluctuating back and forth, depending on the immediate demands of adaptation. Indeed, it must do so, as circumstances of the physical environment—climate and patterns of circulation of ocean currents in the case of cetaceans—and biotic communities—the extinction Mesozoic marine reptiles and the emergence of diatom-based food chains—are dynamic and subject to change. A long-term goal in developing the metrics used here was to develop quantitative data that can be used to determine how extinct cetaceans may have lived. Paleobiologists infer

[35] feeding habits by direct interpretation of the forms of fossil teeth. Our analysis provides a broad, integrated framework of designs in the context of which fossil cetaceans‟ teeth and jaws can be compared with the teeth and jaws of living or fossils forms with feeding habits that are well known. Thus, it provides paleobiologists with an additional tool to use in interpreting modes of adaptations of extinct cetaceans.

ACKNOWLEDGEMENTS I am very grateful for my mentor and research advisor Roger Thomas, who patiently guided me through the more abstract aspects of complexity and its measurement. Additionally, this project would not be off the ground without our receptive hosts at the Smithsonian, David Bohaska and Nicholas Pyenson at the USNM on Constitution Avenue, and Charles Potter and John Ososky at the Suitland off-site facility. Finally, a thank you to John Nance for helping us jumpstart the project by introducing us to cetacean jaws in the collection of the Calvert Marine Museum. I am also grateful to Franklin & Marshall College for financial support by way of a Hackman Scholarship and travel funds to visit museums and present results of this work at a regional meeting of the Geological Society of America, in March, 2011. A last thank you goes out to all the countless friends, family, and peers who have been forced to learn much more about complexity and cetacean evolution than they had ever wished to after being subjected to my rambling conversations.

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APPENDIX A: DATA TABLE OF SPECIES, AGES, AND MEASURES OF COMPLEXITY

Cetacean Species Key Age Ma J # teeth Ct-min Ct=Av(#) Ct-max Av Score Jaw tt ch Jc Index AveShift Irreg Janjucetus hunderi Ju Olig-ch 25 U 8 5 7.4 9 7.4 14 0.128 2.29 6.42 Lit: Fitzgerald (2006) Hadrodelphis calvertense Hd Mio-serr 13 U 17 2 2.4 3 2.4 4 0.041 0.13 0.50 Specimen CMM-V-11 Hd Mio-serr 13 L 19 1 1.5 2 1.5 2 0.020 0.17 0.69

Ambulocetus sp. (natans?) Ab Eoc-lut 47 U 11 1 1.5 2 1.8 6 0.288 1.10 3.65 CMM, cast replica, restored Ab Eoc-lut 47 L 11 1 1.5 2 2.3 7 0.353 1.20 3.99 Also USNM 510796 Basilosaurus cetoides Bs Eoc-pri 36 U 10 1 3.9 6 4.4 10 0.174 1.78 5.64 CMM, skull cast on display, Bs Eoc-pri 36 L 11 2 4.9 7 5.7 13 0.165 1.60 5.32 probably from USNM 11962 Maiacetus inuus Mc Eoc-lut 47.5 U 11 1 2.5 5 2.8 9 0.267 2.00 6.64 CMM, skull reconstr on Mc Eoc-lut 47.5 L 11 1 2.5 4 2.5 6 0.144 0.70 2.33 display, based on GSP-UM 3475a Dorudon atrox Dd Eoc-pri 37 U 10 3 3.6 5 4.1 9 0.167 1.22 3.87 CMM, skull reconstr on display Dd Eoc-pri 37 L 10 1 2.8 4 3.7 8 0.206 1.22 4.13

Pakicetus inachus Pk Eoc-lut 49 U 11 1 2.2 3 2.8 8 0.267 1.40 4.65 Specimen USNM 510827 Pk Eoc-lut 49 L 11 1 3.4 5 3.7 10 0.197 1.30 4.32 Lit: Thewissen, Hussain (1998) Protocetus atavus Pc Eoc-lut 45 U 11 1 2.1 3 2.5 6 0.187 0.70 2.33 Specimen USNM 12339 Prosqualodon davidis Pq Mio-aq 22 U 15 1 1.5 3 1.5 5 0.167 0.46 2.18 USNM 467596 / AMNH 18601 Odobenocetops peruvianus Od Plio-zan 5 U 1 4 4.0 4 4.0 3 0 0.00 0.00 Lit: de Muizon et al. (1999) Zarhachis flagellator Zh Mio-bdg 18 U 85 3 3.0 3 3.0 4 0.004 0.02 0.15 Specimen USNM 10485 Zh Mio-bdg 18 L 71 3 3.0 3 3.0 4 0.005 0.03 0.18

Orcinus orca Oc Plio-Rec 0 U 12 1 1.6 2 1.6 3 0.081 0.55 1.89 USNM, specimen on display Oc Plio-Rec 0 L 12 1 1.3 3 1.3 3 0.127 0.36 1.26

Liolithax pappus Lx Mio-Lang 16 U 25 3 3.0 3 3.0 3 0 0.00 0.00 Type specimen, USNM 15985 Lx Mio-Lang 16 L 26 1 1.0 1 1.0 1 0 0.00 0.00

Llanocetus denticrenatus Lc Eoc-pri 35.5 L 11 0 2.1 4 2.4 7 0.235 0.90 2.99 USNM ##### Homo sapiens H Extant 0 U 8 2 3.0 4 4.0 7 0.190 1.29 Investigators' self-study H Extant 0 L 8 2 3.0 4 4.0 7 0.190 1.29 3.61

Physeter catodon Py Extant 0 L 21 1 3.6 4 3.6 4 0.006 0.35 1.51 Specimen USNM 239284 Mesoplodon grayi Mg Extant 0 L 1 4 4.0 4 5.0 4 0 0.00 0.00 Specimen USNM 49880 Mesoplodon europaeus Me Extant 0 L 1 2 2.0 2 3.0 2 0 0.00 0.00 Specimen USNM 571392

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Mesoplodon layardi My Extant 0 L 1 5 5.0 5 7.0 5 0 0.00 0.00 Specimen USNM 21119 M. carlhubbsi Mh Extant 0 L 1 4 4.0 4 5.0 4 0 0.00 0.00 Specimen USNM ##### Kogia breviceps Kb Extant 0 L 15 2 3.3 4 3.3 4 0.016 0.21 0.82 Specimen USNM 302040 Kogia sima Ks Extant 0 L 10 2 2.5 3 2.5 3 0.022 0.11 0.35 Specimen USNM 504336 Cephalorhynchus eutropia Cp Extant 0 U 32 3 3.9 4 3.9 4 0.001 0.03 0.16 Specimen USNM 395375 Cp Extant 0 L 29 3 3.9 4 3.9 4 0.001 0.04 0.17

Inia geoffrensis Ng Extant 0 U 26 2 2.3 3 2.3 4 0.029 0.12 0.56 Specimen USNM 395614 Ng Extant 0 L 26 2 2.4 4 2.4 4 0.026 0.16 0.74

Pontoporia blainvillei Pb Extant 0 U 57 3 3.0 3 3.0 3 0 0.00 0.00 Specimen USNM ##### Pb Extant 0 L 55 2 2.8 3 2.8 4 0.008 0.06 0.32

Phocoena spinipinnis Ph Extant 0 U 17 2 4.5 5 4.5 5 0.006 0.19 0.75 Specimen USNM 395376 Ph Extant 0 L 20 2 3.8 4 3.8 5 0.018 0.21 0.89

Globicephala sp. Gb Extant 0 L 11 2 2.5 3 2.5 4 0.057 0.30 1.00 Specimen USNM 572003 Tursiops truncates (coastal) Tt Extant 0 U 24 1 2.1 3 2.1 5 0.059 0.39 1.77 Specimen USNM 12274 Tt Extant 0 L 24 1 1.3 2 1.3 3 0.058 0.13 0.59

Monodon monoceros Mm Extant 0 U 1 4 4.0 4 5.0 3 0 0.00 0.00 General literature Mauicetus spp. Mu Olig-ch 24 0 0 0.00 0.00 General literature Balaenoptera musculus Bm Extant 0 0 0 0.00 0.00 General literature Delphinapterus leucas Dp Extant 0 U 9 2 2.0 2 2.0 2 0.000 0.00 – Specimen USNM 305071 Dp Extant 0 L 8 1 1.3 2 1.3 4 0.314 0.71 2.01

Note: The complete data file of observations on which these reduced data are based is included as a separate electronic document on the disk on which this thesis is stored. Appendix B, which follows, represents a sample from this original data file.

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APPENDIX B: TOOTH SPACE – SAMPLE RAW DATA AND COMPILATION

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APPENDIX C: PROJECTED DIETARY HABITS OF EXTANT AND EXTINCT CETACEANS

Original graph showing average number of characters Whales that are known to eat crustaceans. versus irregularity of the tooth set. As most odontocetes are piscivores, no graphical model is needed for fish.

Whales that are known to eat squid. Odontocetes that are known to eat shrimp and krill.

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Whales that are known to eat shellfish. Whales that are known to eat seals, sharks, and other whales.

Whales that are known to have spent at least part of their lives on land, and thus would have preyed on terrestrial animals

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