The Influence of Posture and Brain Size on Foramen Magnum Position in Bats

Home , Foramen magnum, Neurocranium, Orthograde posture

THE INFLUENCE OF POSTURE AND BRAIN SIZE ON FORAMEN MAGNUM POSITION IN BATS

A thesis submitted

to Kent State University in partial

fulfillment of the requirements for the

degree of Master of Arts

Aidan Alifair Ruth

May 2010

Thesis written by

Aidan Alifair Ruth

B.A., The Ohio State University, USA 2008

Approved by

C. Owen Lovejoy______, Advisor

Richard S. Meindl______, Chair, Department of Anthropology

John R. D. Stalvey______, Dean, College of Arts and Sciences

TABLE OF CONTENTS

LIST OF FIGURES ...... V

LIST OF TABLES ...... VI

ACKNOWLEDGEMENTS ...... VII

ABSTRACT………………………………………………………………………………………………………………… IX

CHAPTER 1 INTRODUCTION ...... 1

1.1 Anatomy and Development of the Basicranium ...... 1

1.2 Postural Hypotheses...... 2

1.3 Facial Orientation Hypotheses ...... 3

1.4 Neural Hypotheses ...... 4

1.5 Neural Reorganization ...... 5

1.6 An Integrated Hypothesis ...... 6

1.7 The Chiroptera ...... 7

CHAPTER 2 HYPOTHESES ...... 15

CHAPTER 3 MATERIALS AND METHODS ...... 17

3.1 Data acquisition ...... 17

3.2 Measurements ...... 18

CHAPTER 4 RESULTS ...... 20

4.1 Principal Components Analysis ...... 20

4.2 Correlation Analyses...... 21

4.3 Analysis of Covariance ...... 21

CHAPTER 5 CONCLUSIONS ...... 27

5.1 Foramen magnum position is influenced by neocortex size, but not brain size or posture ...... 27

5.2 Neural Reorganization is consistent with the hominid fossil record ...... 30

APPENDIX A ...... 34

CITED LITERATURE ...... 36

LIST OF FIGURES

Figure 1.1. Weidenreich’s Postural Hypothesis……………….……………………………………………10

Figure 1.2. Lateral Radiographs of Cat, Rat, and Rabbit………………………………………………..11

Figure 1.3. Dabelow’s Facial Orientation Hypothesis…………………………………………………….12

Figure 1.4. Biegert’s Hypothesis for the anterior position of the foramen magnum in

humans…………………………………………………………………………………………………………….13

Figure 1.5. Basal view of Saimiri oerstedii and Alouatta seniculus…………………………………14

Figure 3.1. Measurements used in analysis…………………………………………………………………..19

Figure 4.1. Results of Principal Components Analysis……………………………………………………22

Figure 4.2. Results of Analysis of Covariance: Encephalization Quotient……………………..23

Figure 4.3. Results of Analysis of Covariance: Neocortical Quotient……………………………24

LIST OF TABLES

Table 4.1 Component Loadings...... 23

ACKNOWLEDGEMENTS

My gratitude for the help of many individuals during the completion of this thesis can be described using two principal components. The first component may be described as the “Scientific Support” component. Individuals who load heavily on this component include my advisor, Owen Lovejoy, whose prolific expertise in biological anthropology is truly inspiring; Mary Ann Raghanti, whose knowledge in brain biology is staggering; and Richard Meindl, whose resemblance to an encyclopedia is uncanny.

Also loading heavily on this component are Suzanne McClaren at the Carnegie Museum of Natural History Mammals Section, who allowed me access to her beautifully maintained collections of bats and helped me navigate the city of Pittsburgh, and Andy

Jones at the Cleveland Museum of Natural History, who allowed me access not only to his collection of bird skeletons, but also to a sample of birds to dissect.

The second component of my gratitude may be described as the “Moral

Support” component. A certain degree of colinearity exists between the two components: Dr. Lovejoy loads heavily on this component, for making me feel proud of my work. Dr. Raghanti’s “open door” policy has helped me immeasurably, as has her reminder that there is no crying in science. Dr. Meindl’s reassuring demeanor has helped me remain (relatively) calm through many statistical and academic emergencies.

vii

My parents, Steve Ruth and Carol Goodnight, have been especially supportive during the past two years. Finally, my “Monkey Family,” composed of the other grad students in the anthropology department, has contributed many giggles, long talks, and cups of coffee to this component as well.

Aidan Ruth

19 March 2010, Kent, Ohio

viii

ABSTRACT

An anterior position of the foramen magnum is often cited as a correlate of bipedal posture in hominids. Other investigators (Biegert 1963) have suggested that it more accurately reflects increased encephalization. The present study examines this problem in bats, which most commonly employ an inverted but orthograde posture during rest but all which participate in active flight.

The position of the foramen magnum was evaluated using Bolk’s Basal Index

(1909). A mean Basal Index was obtained for ten species of bat belonging to the pteropodidae subfamily, and twenty belonging to the Phyllostomidae subfamily.

Measures of brain volume and were obtained from Baron (1996) and used to create two different indices of neural organization: An Encephalization Quotient (Brian volume/Body volume) and Neocortical Quotient (Neocortex volume/Telencephalon volume). A strong negative correlation was found between Neocortical Quotient and

Basal Index in both Pteropodidae (r= -.717) and Phyllostomidae (r= -.566), as predicted by Biegert’s hypothesis. A linear model shows an interaction between subfamily and

Neocortical quotient (r2 = .828). Since substantial variation in locomotor pattern and/or posture does not obtain within this group of bats, this confounding variable can be excluded. These data provide strong evidence that the position of the foramen magnum may be used as a potential indicator of neural reorganization (in particular, expansion of

the neocortex), but not as an indicator of posture.

CHAPTER 1

Introduction

An anterior position of the foramen magnum is often cited as an anatomical correlate of bipedal posture in hominids. Because bipedality is considered to be one of the earliest “hallmarks” of the hominidae, it is tempting to infer its presence whenever possible. However, an anterior foramen magnum may not reflect an adaptation to upright walking, but instead increased neocortical volume. This study seeks to explore this issue using data from the order Chiroptera. Chiroptera share many adaptations with primates, especially orbital frontation and a trend toward increased brain size and reorganization. Furthermore, the Chiroptera have abandoned quadrupedal locomotion for flight and have adopted an inverted but orthograde posture when at rest.

1.1 Anatomy and Development of the Basicranium

The skull is a highly integrated structure. It is traditionally divided into three units based on embryonic origins, development, and function: The face, the neurocranium, and the basicranium (Hanken and Hall 1993). The face and neurocranium develop primarily by intramembranous ossification, and their shape is therefore dependent on the soft tissue structures around which they develop (e.g., the brain). The basicranium develops through endochondral ossification, during which a set of cartilaginous precursors is replaced by bone. Growth occurs at synchondroses which resemble the

1 2

growth plates of typical long bones (Hanken and Hall 1993).

The foramen magnum transmits the medulla oblongata and is located in the occipital. The occipital articulates with the sphenoid at the spheno-occipital synchondrosis, and with the right and left temporals at the lambdoid suture. Deposition of bone occurs along the borders of these synchondroses throughout development so that the skull changes shape by means of differential growth at these sites throughout ontogeny.

Though the neurocranium and basicranium are functionally distinct from one another and from the face, they are developmentally integrated. For this reason, development of the basicranium and neurocranium are constrained so that they do not interfere with the functional “modules” of the face (McCollum 1999, McCollum 2008).

1.2 Postural Hypotheses

One of the best-known and often-cited explanations for the anterior position of the foramen magnum is the “postural” hypothesis, which holds that the foramen magnum has been relocated anteriorly in hominids because it allows them to balance the head on top of the spinal column more efficiently (e.g. Bolk 1909, Schultz 1942,

DuBrul 1950). Indeed, Dart's (1925) designation of the Taung Child as a bipedal hominid relied heavily on the anterior position of its foramen magnum relative to those of anthropoid apes of equivalent age.

In most quadrupedal mammals, the head's center of mass lies anterior to the

occipital condyles, while in humans the center of mass lies directly above them (Schultz

1942). Proponents of the postural hypothesis suggest that migration of the occipital condyles closer to the center of mass achieves a more efficient biomechanical state for bipedal locomotion. In order to accomplish this migration, the posterior basicranium

“flexes” in relation to the anterior basicranium (which includes the roofs of the eye orbits). This flexion also relocates the orbits in relation to the foramen magnum and allows the visual field to remain facing forward (Weidenreich 1924)(Fig. 1.1). However, in primates basicranial flexion and orbit orientation vary independently of one another:

Relative brain size is a correlate of basicranial flexion, while the position of the eye orbits is influenced by posture (Strait and Ross 1999).

Contrary to the postural hypothesis, many animals (e.g. birds, kangaroos, giraffes) are able to balance their heads efficiently on top of an erect spine without flexing or otherwise reorganizing their basicrania (deBeer 1947). All vertebrates except certain reptiles and amphibians hold their cervical vertebral column vertically while at rest, despite the outer appearance of the neck (Vidal et al. 1986) (Fig 1.2). These observations make the postural hypothesis an unlikely explanation for the anterior position of the foramen magnum in humans.

1.3 Facial Orientation Hypotheses

While posture alone cannot account for variation in foramen magnum position, it could hypothetically contribute to its anterior position in hominids. Dabelow (1929)

suggested that a reorganization of the skull should only occur along with orthograde postures in animals in which the bony eye orbits are highly convergent upon the midline of the face. Such ventral flexion of the orbital axis (and subsequently, the anterior cranial fossa) could then allow the cerebrum to expand into areas that were previously occupied by facial structures (Fig 1.3). Ross and Ravosa (1993) collected data from lateral radiographs of 68 primate species in order to test the relationship between posture, cranial base flexion, orbital orientation, and brain volume. They found that cranial base flexion is strongly correlated with orbital orientation in platyrrhines (r=

.723), cercopithecines (r= .853), and colobines (r= .784). However, only one group of primates, the atelines (Ateles, Brachyteles, and Lagothrix) shares the complete suite of hypothetically associated features, including a higher degree of basicranial flexion, orbital frontation, and orthograde posture. Instead, they found that increased brain size relative to basicranium length is associated with increased basicranial flexion in several taxonomic levels within haplorrhines, including atelines.

1.4 Neural Hypotheses

The relationship between brain size and foramen magnum position might be a function of the length of the basicranium (Gould 1975, Ross and Ravosa 1939, Strait

1999). The brain sits atop the basicranium, so simple flexion can accommodate a larger brain without having to extend the skull in length or breadth. When the spheno- occipital growth site is ablated prematurely in growing rats, the skull manifests a more

human-like shape, with the foramen magnum more anteriorly positioned (DuBrul and

Laskin 1961). This is the case because the brain continues to expand to its adult size, even after this particular growth site has been excised. Gould's hypothesis predicts that animals with shorter basicrania and larger brains should have more anteriorly positioned foramina magna than animals with longer basicrania and smaller brains. Additionally, increased basicranial flexion co-occurs with shorter basicrania in primates (Ross and

Ravosa 1993), contributing further to the forward migration of the foramen magnum.

Hypotheses which suggest that foramen magnum position is related to expansion of the brain may be supported by data which show that apes are born with anteriorly- positioned foramina magna that migrate posteriorly throughout ontogeny as the body grows larger relative to brain size (Ashton and Zuckerman 1952, Zuckerman 1955,

Ashton and Zuckerman 1955, Jeffrey and Spoor 2002). Humans retain a more anterior position of the foramen magnum than do apes because their brain increases in size throughout ontogeny to a much greater degree than do the brains of apes. At birth, the human brain is 27% of its eventual adult size, while in chimpanzees it is 36% (Robson and

Wood 2008).

1.5 Neural Reorganization

In all animal taxa, an increase in brain size is rarely a simple scaling up of a primitive, small brain. Different regions of the brain have expanded at different rates

(e.g. Rilling 2006, Sherwood et al. 2008). When compared to other regions of the brain,

the neocortex has a particularly positive allometric slope, so that larger brains are composed of a relatively higher proportion of neocortex. Humans have a particularly enlarged neocortex, and evidence suggests that neocortex size influences other regions of the brain as well (Rilling 2006), resulting in more voluntary control of motor activities

(Sherwood et. al 2008). This can be seen in the larger proportion of brain stem composed of descending neocortical projections (Tilney 1928, reviewed in Sherwood et al. 2008).

1.6 An Integrated Hypothesis

Biegert (1963) advanced a hypothesis for the position of the foramen magnum that relies on the interplay between two of the most important functional suites in the animal kingdom: The brain and the masticatory apparatus. Beigert hypothesized that as the size of the masticatory apparatus increases, basicranial flexion decreases, while at the same time, an increase in neocortex size results in an increase in basicranial flexion

(Fig 1.4).

Because the size of the masticatory apparatus scales positively with body size while neocortex volume scales negatively with body size, large animals are expected to have relatively flat basicrania and posteriorly positioned foramina magna when compared with small animals. This relationship can be observed in primates: Large- bodied Alouatta exhibits a more posteriorly-positioned foramen magnum than small- bodied Saimiri (Fig. 1.5).

According to Biegert's hypothesis, specialization of either the masticatory apparatus or the brain will manifest itself in a change in basicranial morphology. This hypothesis is particularly intriguing in light of recent work in developmental biology, which establishes close developmental relationships among the basicranial, neurocranial, and oral modules (McCollum 1994, McCollum 2008).

Evidence from the primate lineage has so far failed to conclusively yield a single mechanism for the anterior migration of the foramen magnum in hominids. This suggests that this morphological shift is probably a highly complex and integrated process with no single underlying cause. However, in order to examine likely hypotheses more clearly, it may be useful to leave the primate order and examine the evidence from animals that share particular adaptive suites with primates, including orbital frontation, abandonment of quadrupedal locomotion or adoption of orthograde posture, and increasing brain size and reorganization. The current study attempts to accomplish this by examining the position of the foramen magnum in the order Chiroptera.

1.7 The Chiroptera

The order Chiroptera is the only group of mammals that participates in active flight. The ability to exploit this niche has enabled them to become phylogenetically diverse and behaviorally disparate. Chiroptera are divided into two suborders which have been distinct since the Eocene: Megachiroptera and Microchiroptera (e.g. Mann

1963, Thewissen and Babcock 1991, Jones et al. 2002; but see Pettigrew 1986, Pettigrew

et al. 1989). The Megachiroptera include Old World fruit bats and flying foxes, which rely primarily on vision to forage for fruit. They occupy the most basal position in the

Chiroptera and are relatively poor flyers. The Microchiroptera are a world-wide radiation which has evolved many different dietary specializations and are more proficient flyers. While many species feed on fruit, nectar, small vertebrates, or even blood, most species of Microchiroptera are insectivorous, and may be again divided into species which glean prey from the surface of the ground or foliage, and those that hunt aerially, capturing flying prey (Eisenberg and Wilson 1978, Baron 1996, Safi and

Dechmann 2004). Most species of microchiroptera have evolved the ability to hunt by echolocation, while only one genus of Megachiroptera (Rousettus) has evolved this ability (Baron 1996).

In this study, we have chosen to focus only on the Pteropodidae and

Phyllostomidae subfamilies. The Pteropodidae includes all Megachiroptera, and is an ideal group for the present study because they are highly encephalized when examined using the regression equation for mammals of a similar size (Baron 1996, Stephan and

Frahm 2003). The Phyllostomidae are an ecologically diverse Neotropical radiation that includes frugivores, insectivores, carnivores, and nectarivores. Phyllostomid bats, or

New World leaf-nosed bats, are so named because of a large, fleshy protuberance on the rostrum, which is thought to play a role in directing echolocation (Arita 1990). They almost certainly formed a distinct clade before the Oligocene and were able to exploit feeding niches in the New World that paralleled those occupied by the Megachiroptera

in the Old World (Eisenberg and Wilson 1978, Jones et al. 2002). Because of the wide diversity in habitat and ecological niche, this subfamily displays differences in brain organization that correspond to their different foraging strategies (Eisenberg and Wilson

1978, Safi and Dechmann 2004, Shumway 2008). In Chiroptera, enlargement of the neocortex may reflect an increasingly complex ecological niche (Eisenberg and Wilson

1978, Safi and Dechmann 2004, Ratcliffe et al. 2005, Shumway 2008). Location of energy-rich foods, which are temporally and spatially patchy (such as fruit and nectar), requires complex cognitive and sensory capacities. Such needs are reflected in the enlarged neocortex of the Pteropodidae and certain subfamilies of Phyllostomidae

(Eisenberg and Wilson 1978). Conversely, in insectivorous bats, which are highly specialized for flight (such as the Phyllostomid genera Mimon and Lonchorina), enlargement of the neocortex has been selected against (Mann 1963). This may be because the use of echolocation as a primary foraging strategy requires little neocortical volume (Eisenberg and Wilson 1978). These species may instead demonstrate enlargement in regions of the brain that are connected with auditory processing, such as the inferior colliculi.

Figure 1.1 Weidenreich’s Postural Hypothesis for the position of the foramen magnum. A biomechanically efficient posture in bipedal humans is achieved by a posterior “flexion” of the basicranium in relation to its anterior portion. This includes the roof of the eye orbits (illustrated by angle B). Such flexion also relocates the orbits in relation to the foramen magnum (illustrated by angle A) and allows the visual field to remain facing forward (Weidenreich 1924).

Figure 1.2 Lateral radiographs from (A) cat, (B) rat, and (C) rabbit. Note the vertical orientation of the cervical vertebral column, despite the orientation of the soft tissue surrounding it. From Vidal et al 1986.

Figure 1.2. Dabelow’s Facial Orientation Hypothesis for the Position of the foramen magnum. As the eyes approximate the midline of the face (Indicated by “A” arrows), the neurocranium can expand ventrally (indicated by “B” arrows), and the foramen magnum will migrate anteriorly (indicated by “C” arrow).

Figure 1.4 Biegert’s hypothesis for the anterior position of the foramen magnum in humans. The foramen magnum relocates anteriorly in species which possess a large neocortex, but posteriorly in species which possess a large masticatory apparatus.

Figure 1.5. Basal view of Saimiri oerstedii (top) and Alouatta seniculus (bottom). Biegert’s (1963) hypothesis can be interpreted as an essentially allometric hypothesis. The masticatory apparatus exhibits positive allometry, while the neocortex exhibits negative allometry. Thus, as body size increases, the masticatory apparatus will also increase in size and the foramen magnum will relocate posteriorly. Note the anterior position of the foramen magnum in small-bodied Saimiri (Brain weight 24,000 mg; Body weight 660 grams) when compared with large-bodied Alouatta (Brain weight 52,000 mg; Body weight 64,000 g). Drawn from Carnegie MNH 1588 and 2722.

CHAPTER 2

Hypotheses

The present study examines neural hypotheses for the position of the foramen magnum in the order Chiroptera. Bats do not vary considerably with regard to locomotor habitus, so in theory, significant differences in foramen magnum position may falsify postural hypotheses for its differential position in various taxa. Similarly, facial prognathism and orbital orientation vary little in Chiroptera, so the effect of neural expansion and reorganization may be tested in relative isolation.

Hypothesis 1: The foramen magnum is positioned more anteriorly in species with a higher ratio of brain size to body size.

The neural hypothesis of Gould (1975) predicts that the foramen magnum will be positioned more anteriorly in more highly encephalized bats as the result of a shortened and more flexed basicranium. Basal Index (an indicator of foramen magnum position) will be negatively correlated with Encephalization Quotient (an indicator of brain size relative to body size).

Hypothesis 2: The foramen magnum is positioned more anteriorly in species in which a greater portion of the telencephalon is composed of neocortex

The neural hypothesis of Biegert (1963) proposes that expansion of the neocortex relative to the rest of the brain results in vaulting of the occipital region and 15 16

forces the foramen magnum into a more anterior position. Basal Index will be negatively correlated with Neocortical Quotient (an indicator of neocortical expansion in relation to the telencephalon). Hypothesis 2 differs from hypothesis 1 in that it explores the relationship of neural reorganization that may have taken place in bats to foramen magnum position.

CHAPTER 3

Materials and Methods

3.1 Data acquisition

Specimens were selected from the research collections in the Mammals Section at the Carnegie Museum of Natural History. Individuals with noticeable skeletal injury or post-mortem damage were excluded from analysis. In order to control for the effects of developmental ontogeny, only adult bats were used, as determined by the absence of visible cranial vault sutures (Gianni et al. 2006). At least three specimens were photographed from each species. Sex of the individual was not available in all cases, but in species in which a notable difference in brain weight was noted between sexes, only males were included in the analysis.

A Nikon Coolpix S550 10 megapixel digital camera was mounted on a tripod and positioned perpendicular to the table surface, 20 cm away from each cranium. A scale was placed perpendicular to the camera’s line of sight, and in line with the midline of the skull. Skulls were positioned in the Frankfort Horizontal plane by sight and photographs were taken in norma basilaris.

Measurements of brain weight, body weight, telencephalon volume and neocortex volume were obtained from Baron (1996).

17 18

3.2 Measurements

The following cords were drawn on each image using the ImageJ “draw” function:

1. A cord connecting right and left poria 2. A cord connecting right and left foramina ovale 3. A cord connecting the right and left zygoma

The following eleven measurements were taken from each norma basilaris image using the ImageJ “measure” function after each image had been adjusted to scale:

1. Distance from basion to the bizygomatic cord, B-BZ 2. Distance from basion to occipiton, B-O 3. Distance from basion to prosthion, B-PR 4. Maximum skull breadth, MSB 5. Distance from occipiton to prosthion (maximum skull length), O-PR 6. Distance between right and left poria, PO-PO 7. Distance between right and left foramina ovale, OV-OV 8. Distance from basion to Biporion chord, B-BP 9. Distance between basion and the foramina ovale chord, B-OV 10. Length of foramen magnum, FML 11. Breadth of foramen magnum, FMB

For each species, a mean was taken for each of the above measurements. A Basal Index

(BI) was obtained by dividing B-BZ/B-O and was calculated to serve as a measure of foramen magnum placement on the anteroposterior axis (Bolk 1909). An

Encephalization Quotient (EQ) was obtained by dividing the brain weight in mg by body weight in grams (both obtained from Baron 1996). A Neocortical Quotient, which serves as a measurement of brain reorganization with relation to the neocortex, was obtained by dividing neocortex volume by telencephalon volume (both from Baron 1996). (See

Appendix A).

1 cm

Figure 3.1 Measurements used in Analysis.

CHAPTER 4

Results

Only species for which more than 3 individuals were available were used in statistical analyses, which were conducted using SPSS v. 17.0. The analyses were chosen to answer three questions: (1) Does variation exist in the position of the foramen magnum in Chiroptera? If so, can it be accounted for by differences in (2) brain size

(Hypothesis 1 from Chapter 2) or (3) neural reorganization (Hypothesis 2 from Chapter

2)?

4.1 Principal Components Analysis

As in any biological system, many cranial measurements are largely redundant.

In order to determine how many genuine dimensions of variation exist in the data set, measurements for N cases were analyzed by using a multivariate principal components analysis (PCA). Results are shown in Figure 4.1 and Table 4.1. Two principal components emerge, the first of which accounts for 63% of the variation in the sample, but fails to distinguish between any particular group. All measurements save B-O load heavily on this axis. It appears to reflect variation in skull morphology dependent principally on differences in overall body size.

The second component accounts for 24% of the overall variation present in the sample, and appears to reflect the length of the occiput. The distance from Basion to

20 21

occipiton and foramen magnum length load heavily on the second component, but variables relating to more direct measures of body size or size of the face do not.

Together, the first and second components account for 87% of the total variation present in the sample. This suggests that there are only two true dimensions of variation in the suite of measurements used, as addition of additional components could explain only an additional 6% of the overall variation.

4.2 Correlation Analyses

For each subfamily of bats, correlation analyses were performed between the

Basal Index and both Encephalization Quotient (EQ) and Neocortical Quotient (NQ). EQ by itself is not found to be a correlate of the Basal Index. However, NQ is substantially and negatively correlated with Basal Index in both subfamilies (Phyllostomidae: r= -.566, p<.005, n= 20; Pteropodidae r= -.717, p < .01, n= 10). That is, as the NQ increases the

Basal Index decreases, indicating an anterior position of the foramen magnum.

4.3 A Linear Model

In order to quantify the impact of subfamily on the relationship between the neural quotients and Basal Index, the data were analyzed by an Analysis of Covariance.

The regression equation

BI= 5.71 – 0.055 (EQ) has an r2 value of only .03 (Fig 4.2) and shows no interaction between subfamily and EQ.

The regression equation

BI = 46.889 – 81.013 (NQ) - 41.358 (Subfamily) +75.659 (Interaction term) shows an interaction between subfamily and NQ, so that a difference in the slope of the regression line exists between the two subfamilies (r2 = .828) for NQ (Fig. 4.3).

Figure 4.1 Results of Principal Components Analysis. Principal components analysis shows that clades are not distinguished from one another on PC1, which appears to reflect cranial variation resulting from variation in body size. Pteropodidae and Phyllostomidae are distinguished from one another on PC2, which appears to reflect the length of the occiput. Subfamilies of the Phyllostomidae (Glossophaginae, Phyllostominae, Stenoderminae, and Sturinurinaeare) are represented by solid symbols, while those belonging to the Pteropodidae (Macroglossinae and Pteropodinae) are represented by open symbols.

Table 4.1 Component Loadings. Component 1 accounts for 63% of the variation present in the model, while component 2 accounts for an additional 24%. Addition of the third component only adds 6% to the total explained variance and is not included in analysis.

Figure 4.2 Analysis of Covariance: Encephalization Quotient. The equation BI= 5.71 – 0.055 (EQ) shows no interaction between subfamily and EQ (r2= .030). Pteropodid bats are indicated by open squares and Phyllostomid bats are indicated by closed circles.

Figure 4.3 Analysis of Covariance: Neocortical Quotient. The equation BI= 46.889 – 81.013 (NQ) - 41.358 (Subfamily) +75.659 (Interaction term) shows that the slopes of the regression lines are different in two families of bat. Pteropodid bats are indicated by open squares and Phyllostomid bats are indicated by closed circles.

CHAPTER 5

Discussion

5.1 Foramen magnum position is influenced by neocortex size, but not brain size or

posture

Results indicate that an anterior position of the foramen magnum is correlated with an increase in neocortex volume, but not with an overall increase in encephalization. These results strongly support Biegert’s (1963) hypothesis (hypothesis

2 in Chapter 2).

As the neocortex expands, it can do so in any direction except anteriorly.

Expansion of the brain cannot occur toward the anterior of the skull because of the functional and developmental commitment of this space to the nasal, oral, and visual modules (McCollum 1999). As a result, any neocortical expansion must occur into the vertex and posterior of the skull, increasing the length of the occiput and moving the foramen magnum into a relatively more anterior position.

That neocortex expansion is more highly correlated with foramen magnum position than gross encephalization relative to body size is surprising because of the strong relationship between encephalization and increased neocortical volume

(Sherwood et. al 2008). However, simple brain volume and cranial capacity have long been recognized as problematic parameters for measuring intelligence and other

27 28

behavioral characters relating to the neocortex. Individuals afflicted by Primary

Microcephaly possess brains that are only 400-600 cubic centimeters in volume, but still retain many of the behavioral hallmarks of our species (Holloway 1966). This suggests that, though they lack the high encephalization quotient typical of non-pathological humans, their neural organization affords them relative behavioral near-normalcy.

Other species that have highly specialized sensory suites may display an increase in encephalization without any corresponding increase in neocortical volume. While birds do not possess a true laminated neocortex, they do have a homologous region of the pallium called the nidopallium caudolaterale. The nidopallium caudolaterale comprises much of the volume of the forebrain and develops from the same telencephalic origins as the neocortex (Güntürkün 2005, Kirsch et al. 2008). While a complete data set has not been collected, preliminary observations show that in animals in which the pallium is expanded (such as the blue jay and other corvids (Altmann 1945)) the foramen magnum is located relatively anteriorly. Owls possess high encephalization quotients (Altmann 1945). However, this may be because they possess a remarkably large functional analog of the mammalian primary visual cortex called the avian visual wulst (e.g. Pettigrew and Konishi 1976). As a result, they have a much higher encephalization quotient than would be predicted from allometric scaling with pallium size. The foramen magnum in owls is anteriorly positioned, but the entire basicranium is extremely short anterio-posteriorly.

In dolphins, the paleocortex occupies a much higher percentage of the overall brain than in other mammals, which is most likely the result of their incredibly sophisticated biosonar (e.g. Marino et al. 2004, Oelschlager et al. 2007). Lost in gross percentages is the observation that, though the neocortex occupies a relatively lower percentage in dolphins than in other mammals, both their paleocortex and neocortex are, in fact, exceptionally large. Nevertheless, their foramen magnum lies relatively posteriorly. In essence, foramen magnum position is largely posteriorized in dolphins, not because of a small neocortex, but rather as a consequence of such a large paleocortex.

A similar phenomenon may be at work in bats, whose foraging strategy relies heavily on visual and auditory signals from their environment (Eisenberg and Wilson

1978, Safi and Dechmann 2004). These may have selected for an expansion of the thalamus (which develops from the diencephalon) or the inferior and superior colliculi

(which develop from the mesencephalon)(Safi and Dechmann 2004). Expansion of either of these functional suites would increase the encephalization quotient of the animal. However, expansion in these areas would not result in an anterior migration of the foramen magnum, and in fact might result in posterior migration of the foramen magnum, as they occur anterior to the brain stem.

5.2 Neural Reorganization is consistent with the hominid fossil record

Though fossils which preserve information about the neurology of ancient hominids are exceedingly rare, two endocasts exist which demonstrate that early hominids exhibited a human-like neural organization, despite a relatively small cranial capacity (Holloway 2004). The Taung endocast (Dart 1925) preserves the lunate sulcus

(Holloway 1969, Holloway et al. 2004, but see Falk 2007), which occupies a more posterior position than is present in extant monkeys. In humans, when the lunate sulcus is present, it shares this posterior position (Holloway 1969). This may indicate that in Australopithecus africanus, the neocortex had increased in size relative to the adjacent posterior visual cortex. An endocast attributed to an adult Australopithecus africanus individual (STW 505) preserves the lunate sulcus and demonstrates a similar posterior position (Holloway et. al 2004).1

The fossil record of skulls preserving foramina magna is relatively more prolific than the record of endocasts. Fossils attributed to Homo erectus preserve foramina

1 Despite a large body of literature published on fossil endocasts, many neurologists hold that gross anatomy of the brain is uninformative with regard to neural reorganization, and that histological and functional imaging studies are the only rigorous way to distinguish different areas of the brain from one another (Holloway 1966,

Holloway 2002, Preuss 2001, Preuss 2006).

magna which lie approximately on the bitympanic line, which is the condition seen in modern Homo sapiens (Dean and Wood 1981). In earlier fossils, such as those attributed to Au. africanus (Sts 5, Sts 19, Sts 25, MLD 37/38), the foramen magnum lies posterior to the bitympanic line, but is more anterior than is seen in extant apes (Dean and Wood 1981, Ahern 2005). Even the earliest fossils attributed to the hominid lineage preserve a position anterior to that seen in extant apes. Ardipithecus ramidus (ARA-VP

1/500) preserves the foramen magnum position in relation to the carotid foramen, and is distinguished from Pan but not from early hominids by the size of this separation

(Suwa et al. 2009). Sahelanthropus tchadensis shares this condition (Brunet et al 2004).

Many of these fossils do not possess a cranial capacity exceeding those of extant apes

(Holloway 1969), but if neural reorganization is reflected by the position of the foramen magnum, these observations support the hypothesis that the brain was reorganized prior to expansion in the hominid lineage.

It is notable that Ar. ramidus is at least partially arboreal (White et al. 2009,

Lovejoy et al. 2009), but still demonstrates an anterior position of the foramen magnum. Were the relocation of the foramen magnum an adaptation to upright walking, it should occur as a refinement of an established set of adaptations related to locomotion and would only be apparent in a particular taxon after it has become fully adapted to upright walking. If the anterior position of the foramen magnum is to be accounted for as an adaptation to locomotion, its appearance so early in the sequence of evolutionary events leading to habitual upright walking is unexpected.

In fossils attributed to the Au. boisei and robustus (KNM-ER 406, OH 5, and

SK47), the foramen magnum lies anterior to the bitympanic line, even more so than in modern H. sapiens. The robust australopithecines did not presumably possess a larger neocortex than modern humans, but rather a reduced anterior dentition. Since the reduction of the anterior dentition results in reduced prognathism, this may be consistent with Biegert’s hypothesis that neocortex expansion and the size of the masticatory apparatus both simultaneously influence the position of the foramen magnum. However, the extremely large posterior dentition in the robust australopithecines may confound this explanation.

CHAPTER 6

Conclusions

In Chiroptera, a more anteriorly positioned foramen magnum appears to be a function of increased neocortical volume. Neocortical expansion may reflect adaptation to a complex ecological niche, requiring cognitive elaboration and amplification of sensory specializations such as vision.

These observations from Chiroptera are relevant to the human fossil record.

They show that foramen magnum position is probably not informative with regard to posture or locomotion, and that inferences with respect to bipedality must be made instead from the postcranium. However, foramen magnum position may reflect the profound increase in neocortical volume and neural reorganization that is typical of the human lineage. If this is indeed the case, foramen magnum position serves as a viable indicator of brain expansion in the fossil record, and might be more reliable in that regard than are exceptionally small samples of endocranial volume.

APPENDIX A

Basal Index, Encephalization Quotient, and Neocortical Quotient for species used in analysis. Subfamily Species Basal Index Encephalization Neocortical Quotient Quotient Pteropodidae Cynopterus 6.28 28.94 .47 brachyotis Cynopterus 6.78 23.19 .48 sphinx Hypsignathus 2.14 11.22 .54 monstrous Eidolon helvum 4.86 16.37 .52 Eonycterus 7.37 22.32 .48 splea Epomorphus 8.76 24.82 .49 labiatus Micropteropus 8.23 32.91 .49 pusillus Myonycterus 6.38 31.79 .49 torquata Rousettus 5.96 16.74 .50 aegyptiacus Epomops 10.14 18.42 .49 franqueti Stenoderminae Artibeus 3.02 32.63 .45 concolor Artibeus 2.72 37.06 .47 cinereus Artibeus 2.78 24.78 .49 jamaicensis Artibeus 2.81 22.02 .47 lituratus Artibeus harti 3.32 31.74 .46 Chiroderma 3.32 28.47 .51 villosum Uroderma 2.63 37.78 .46 bilobatum 34 35

Carolliinae Carollia 2.65 30.67 .43 perspiculata Glossophaginae Glossiphaga 3.69 38.50 .42 longirostrus Glossiphaga 3.98 39.70 .44 soricina Phyllostominae Mimon 2.14 27.63 .54 crenulatum Phyllostomus 3.01 29.78 .50 discolor Phyllostomus 2.65 19.71 .51 elongatus Tonatia 2.06 23.41 .63 sylvicola Tonatia bidens 2.57 26.80 .50 Trachops 3.10 27.18 .57 cirrhosus Sturnirinae Sturnia ludovici 3.11 26.10 .43 Sturnia tildae 3.14 28.73 .46

CITED LITERATURE

Ahern, JC. 2005. Foramen magnum position variation in Pan troglodytes, Plio-Pleistocene hominids, and recent Homo sapiens: Implications for recognizing the earliest hominids. American Journal of Physical Anthropology, 127: 267-276

Aiello L and Dean C. 2002. An Introduction to Human Evolutionary Anatomy. Academic Press. Arita HT. 1990. Noseleaf Morphology and Ecological Correlates in Phyllostomid Bats. Journal of Mammalogy, 71:36-47. Ashton EH and Zuckerman S. 1952. Age changes in the position of the occipital condyles in the chimpanzee and gorilla. American Journal of Physical Anthropology, 10:277-288. Ashton EH and Zuckerman S. 1956. Age changes in the position of the foramen magnum in hominoids. Proceedings of the Zoological Society of London, 126:315-326.

Bailey W, Slightom J, and Goodman M. 1992. Rejection of the "flying primate" hypothesis by phylogenetic evidence from the epsilon-globin gene. Science, 256:86-89. Baron G, Stephan H, and Frahm H. 2003. Comparative Neurobiology in Chiroptera (1st ed.). Birkhäuser Basel. Biegert J. 1963. The evaluation of characteristics of the skull, hands and feet for primate taxonomy. In: Washburn SL , editor. Classification and human evolution. Chicago: Aldine. p 116-145.

Bolk L. 1909. On the position and displacement of the Foramen magnum in the Primates. Verh Akad Wet Amst, 12:525-534. Brunet M, Guy F, Pilbeam D, Mackaye HT, Likius A, Ahounta D. 2002. A new hominid from the

Upper Miocene of Chad, Central Africa. Nature, 418:145-151.

36 37

Dabelow A. 1929. Uber Korrelationen in der phylogenetischen Entwicklung der Schadelform. II. Beziehungen zwuschen Gehirn und Schadelbasisform bei den Mammaliern. Gegenbaurs Morphol Jahrb 67:84–133. Dart RA. 1925. Australopithecus africanus: the man-ape of South Africa. Nature 115:195-199. Dean MC, and Wood BA. 1981. Metrical analysis of the basicranium of extant hominoids and Australopithecus. American Journal of Physical Anthropology, 54:63-71. de Beer GR. 1947. How animals hold their heads. Proc Linn Soc London 159: 125–139 Dechmann DKN and Safi K. 2009. Comparative studies of brain evolution: a critical insight from the Chiroptera. Biological Reviews, 84:161-172. DuBrul EL. 1950. Posture, locomotion and the skull in Lagomorpha. The American Journal of Anatomy, 87:277-313. DuBrul EL. 1977. Origin of the speech apparatus and its reconstruction in fossils. Brain and Language, 4:365-381.

DuBrul EL. 1977. Early hominid feeding mechanisms. American Journal of Physical Anthropology, 47:305-320. DuBrul EL and Laskin DM. 1961. Preadaptive potentialities of the mammalian skull: an experiment in growth and form. The American Journal of Anatomy, 109:117-132.

Eisenberg, JF and Wilson DE. 1978. Relative Brain Size and Feeding Strategies in the Chiroptera. Evolution, 32:740-751. Falk D. 2007. Brief Communication: New Reconstruction of the Taung Endocast. American

Journal of Physical Anthropology, 134:529-534. Giannini NP, Wible JR and Simmons NB. 2006. On the Cranial Osteology of Chiroptera. I. Pteropus (Megachiroptera: Pteropodidae). Bulletin of the American Museum of Natural History, 295:1-134.

Gould SJ. 1994. Hen's Teeth and Horse's Toes: Further Reflections in Natural History. W. W. Norton & Company. Gould SJ. 1977. Ontogeny and phylogeny. Harvard University Press. Gould SJ. 1975. Allometry in Primates, with Emphasis on Scaling and the Evolution of the Brain. In Approaches to Primate Paleobiology. Contrib. Primat. 5:244-292. Gray H. 1974. Gray's Anatomy: The Unabridged Running Press Edition Of The American Classic

(Unabridged.). Running Press. Güntürkün O. 2005. The avian `prefrontal cortex' and cognition. Current Opinion in Neurobiology 15:686-693. Hanken J and Hall BK. 1993a. The Skull, Volume 1: Development (1st ed.). University Of Chicago Press. Hanken J and Hall BK. 1993b. The Skull, Volume 2: Patterns of Structural and Systematic Diversity (1st ed.). University Of Chicago Press.

Holloway RL. 1966. Cranial Capacity, Neural Reorganization, and Hominid Evolution: A Search for More Suitable Parameters. American Anthropologist, New Series, 68:103-121. Holloway RL (2002) Brief communication: how much larger is the relative volume of area 10 of the prefrontal cortex in humans? American Journal of Physical Anthropology 118:399-

401. Holloway RL, Clarke RJ, and Tobias PV. 2004. Posterior lunate sulcus in Australopithecus africanus: was Dart right? Comptes Rendus Palevol

Hutcheon JM, Kirsch JA, and Garland Jr T. 2002. A Comparative Analysis of Brain Size in Relation to Foraging Ecology and Phylogeny in the Chiroptera. Brain, Behavior and Evolution, 60:165-180.

Jarvis, E. D., Gunturkun, O., Bruce, L., Csillag, A., Karten, H., Kuenzel, W., et al. (2005). Avian brains and a new understanding of vertebrate brain evolution. Nat Rev Neurosci, 6(2), 151-159. doi: 10.1038/nrn1606 Jeffery N. 2002. Differential regional brain growth and rotation of the prenatal human tentorium cerebelli. Journal of Anatomy, 200:135-144. Jeffery N, and Spoor F. 2004. Ossification and midline shape changes of the human fetal cranial

base. American Journal of Physical Anthropology, 123:78-90. Jones KE, Purvis A, MacLarnon A, Bininda-Edmods ORP, and Simmons NB. 2002. A Phylogenetic Supertree of the Bats (Mammalia: Chiroptera). Biological Reviews, 77:223-259. Lieberman DE, McCarthy RC, Hiiemae KM, and Palmer JB. 2001. Ontogeny of postnatal hyoid and larynx descent in humans. Archives of Oral Biology 46:117 - 128. Lovejoy CO, Simpson SW, White TD, Asfaw B, Suwa G. 2009. Careful Climbing in the Miocene: The forelimbs of Ardipithecus ramidus and Humans are primitive. Science 326:70

Luboga SA and Wood BA. 1990. Position and orientation of the foramen magnum in higher primates. American Journal of Physical Anthropology, 81:67-76. Mann G. 1963. Phylogeny and Cortical Evolution in Chiroptera. Evolution 17:589-591. Marino L, Sudheimer KD, Murphy TL, Davis, KK, Pabst DA McLellan WA. 2001. Anatomy and

three-dimensional reconstructions of the brain of a bottlenose dolphin (Tursiops truncatus) from magnetic resonance images. The Anatomical Record 264:397-414. McCollum MA. 1994. Mechanical and spatial determinants of Paranthropus facial form.

American Journal of Physical Anthropology 93:259-273. McCollum MA. 1999. The Robust Australopithecine Face: A Morphogenetic Perspective. Science 284:301-305. McCollum MA. 2008. Nasomaxillary remodeling and facial form in robust Australopithecus: a reassessment. Journal of Human Evolution 54:2-14.

Monteiro-Filho ELDA, Monteiro LR, and Reis SFD. 2002. Skull Shape and Size Divergence in Dolphins of the Genus Sotalia: A Tridimensional Morphometric Analysis. Journal of Mammalogy 83:125-134. Oelschlager HH, Haas-Rioth M, Fung C, Ridgway S, and Knauth M. 2008. Morphology and Evolutionary Biology of the Dolphin (Delphinus sp.) Brain- MR Imaging and Conventional Histology. Brain, Behavior and Evolution 71:68-86.

Pettigrew JD, Jamieson BGM, Robson SK, Hall LS, McAnally KI, & Cooper HM. 1989. Phylogenetic Relations Between Microbats, Megabats and Primates (Mammalia: Chiroptera and Primates). Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 325:489-559. Pettigrew JD. 1986. Flying primates? Megabats have the advanced pathway from eye to midbrain. Science 231:1304-1306. Pettigrew JD. 1991. Wings or Brain? Convergent Evolution in the Origins of Bats. Systematic

Zoology 40:199-216. Pettigrew JD and Konishi M. 1976. Effect of monocular deprivation on binocular neurones in the owl's visual Wulst. Nature264:753-754. Pitnick S, Jones KE, and Wilkinson GS. 2006. Mating system and brain size in bats. Proceedings

of the Royal Society B: Biological Sciences 273:719-724. Preuss TM, 2001. The discovery of cerebral diversity: An unwelcome scientific revolution. In D. Falk and K. Gibson (eds.): Evolutionary Anatomy of the Primate Cerebral Cortex.

Cambridge: Cambridge University Press, pp. 138-164. Preuss T. 2006. Who's afraid of Homo sapiens? Journal of Biomedical Discovery and Collaboration 1:17. Ratcliffe JM, Fenton MB, and Shettleworth SJ. 2006. Behavioral Flexibility Positively Correlated with Relative Brain Volume in Predatory Bats. Brain, Behavior and Evolution 67:165-176.

Rilling JK. 2006. Human and nonhuman primate brains: Are they allometrically scaled versions of the same design? Evolutionary Anthropology: Issues, News, and Reviews15:65-77. Robson SL and Wood B. 2008. Hominin life history: reconstruction and evolution. Journal of Anatomy 212:394-425. Ross C, and Henneberg M. 1995. Basicranial flexion, relative brain size, and facial kyphosis in Homo sapiens and some fossil hominids. American Journal of Physical Anthropology

98:575-593. Ross CF and Ravosa MJ. 1993. Basicranial flexion, relative brain size, and facial kyphosis in nonhuman primates. American Journal of Physical Anthropology 91:305-324. Safi K and Dechmann DKN. Adaptation of brain regions to habitat complexity: a comparative analysis in bats (Chiroptera). Proceedings of the Royal Society B: Biological Sciences 272:179-186. Satoh K and Iwaku F. 2008. Foramen magnum angle and its effect on visual field in two

Apodemus murids. Mammal Study 33:151-155. Shumway CA. 2008. Habitat Complexity, Brain, and Behavior. Brain, Behavior and Evolution 72:123-134. Sherwood CC, Subiaul F, and Zawidzki TW. 2008. A natural history of the human mind: tracing

evolutionary changes in brain and cognition. Journal of Anatomy 212:426-454. Schultz AH. 1942. Conditions for balancing the head in primates. American Journal of Physical Anthropology 29:483-497.

Spoor F. 1997. Basicranial architecture and relative brain size of Sts 5 (Australopithecus africanus) and other fossil hominids. South African Journal of Science 93:182-186. Stephan H, and Pirlot P. 1970. Volumetric Comparisons of Brain Structures in Bats. Journal of Zoological Systematics and Evolutionary Research 8:200-236.

Strait DS. 1999. The scaling of basicranial flexion and length. Journal of Human Evolution 37:701-719. Strait DS and Ross CF. 1999. Kinematic data on primate head and neck posture: Implications for the evolution of basicranial flexion and an evaluation of registration planes used in paleoanthropology. American Journal of Physical Anthropology 108:205-222. Striedter GF. 2004. Principles of Brain Evolution (1st ed.).

Suwa G, Asfaw B, Kono RT, Kubo D, Lovejoy CO, and White TD. 2009. The Ardipithecus ramidus Skull and Its Implications for Hominid Origins. Science 236:68-687. Thewissen JGM and Babcock SK. 1992. The Origin of Flight in Bats. BioScience 42:340-345. Thewissen JGM and Babcock SK. 1991. Distinctive cranial and cervical innervation of wing muscles: new evidence for bat monophyly. Science 251:934-936. Vidal PP, Graf W, and Berthoz A. 1986. The orientation of the cervical vertebral column in unrestrained awake animals. Experimental Brain Research 61:549-559.

Weidenreich F. 1941. The Brain and Its Role in the Phylogenetic Transformation of the Human Skull. Transactions of the American Philosophical Society, New Series 31:320-442. White TD, Asfaw B, Beyene Y, Haile-Selassie Y, Lovejoy CO, Suwa G, WoldeGabriel G. 2009. Ardipithecus ramidus and the Paleobiology of Early Hominids. Science 326:75-86.

Zuckerman S. 1955. Age changes in the basicranial axis of the human skull. American Journal of Physical Anthropology 13:521-539.