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The Pennsylvania State University The Pennsylvania State University The Graduate School Department of Anthropology VARIATION IN PISIFORM MORPHOLOGY A Thesis in Anthropology by Lia Michelle Gavazzi 2017 Lia Michelle Gavazzi Submitted in Partial Fulfillment of the Requirements for the Degree of Master of Arts December 2017 ii The thesis of Lia Michelle Gavazzi was reviewed and approved* by the following: Timothy Ryan Associate Professor of Anthropology Thesis Co-Adviser Philip L. Reno Associate Professor of Anatomy Philadelphia College of Osteopathic Medicine Thesis Co-Adviser Kenneth Hirth Professor of Anthropology Director of Graduate Studies, Department of Anthropology *Signatures are on file in the Graduate School iii ABSTRACT The pisiform is unique among carpal bones because it is the only one to form a secondary center of ossification and growth plate, a configuration that is present across nearly all mammalian lineages. The human pisiform has undergone major morphological changes including the lost of its growth plate and an ossification center. What is typically a rod-shaped bone in many mammalian species is more akin to a pea shape in our species. This drastic change in development and morphology has a number of implications for humans, however the functional consequences of pisiform growth plate loss are still not understood. The pisiform is severely underrepresented in most skeletal literature, despite its relative importance. Unique human pisiform morphology is often correlated to locomotor behaviors or tool use, although direct associations between carpal morphology and specific behaviors have yet to be established. To understand the developmental history of the pisiform, it is imperative to look beyond the scope of mammals. Investigation of reptilian and amphibious species reveal a complicated and non-linear developmental history of the pisiform. Evolutionary research frequently relies on a diverse number of species to act as proxy for the subject of interest. In the context of development, it is beneficial to compare species across multiple taxa with similar skeletal morphology to identify similarities or differences in development trajectories. In a remarkable case of parallel evolution, the family Xenarthra, comprised of sloths, armadillos, and anteaters contains several species who share morphological similarities with extant hominoids. This includes a reduced pisiform in each species of extant sloths. Our research indicates that the giant anteater pisiform develops along a typical mammal trajectory with the secondary center of ossification and a growth plate. The two-toed and three- toed sloth pisiform does not indicate any secondary center in ontogeny, leading us to conclude that the growth plate has additionally been lost in these species. iv TABLE OF CONTENTS List of Figures ......................................................................................................................... v List of Tables ........................................................................................................................... vi Acknowledgements .................................................................................................................. vii Chapter 1 A review of bone biology and growth plate formation ........................................... 1 Bone and growth plate development ................................................................................ 2 Wrist Anatomy and Pisiform Morphology ...................................................................... 8 Citations ........................................................................................................................... 11 Chapter 2 Tetrapod Pisiform Ossification Patterns .................................................................. 14 The fin-to-limb transition ................................................................................................. 14 Methods and Results ........................................................................................................ 15 Amphibians .............................................................................................................. 17 Reptiles ..................................................................................................................... 19 Mammals .................................................................................................................. 23 Conclusion and Discussion .............................................................................................. 24 Citations: .......................................................................................................................... 26 Chapter 3 Xenarthran Pisiform Morphology and Comparison with Hominoid Species .......... 28 Lorisine and Xenarthran Evolutionary History ................................................................ 29 Lorisine Evolutionary History .................................................................................. 29 Two-Toed and Three-Toed Sloth Evolutionary History .......................................... 33 Hominoid evolution ......................................................................................................... 33 Methods ............................................................................................................................ 38 Lorisoidea......................................................................................................................... 39 Galago ...................................................................................................................... 39 Lorises ...................................................................................................................... 40 Xenarthan Development .................................................................................................. 43 Giant Anteater .......................................................................................................... 43 Sloths ........................................................................................................................ 44 Discussion ........................................................................................................................ 46 Citations ........................................................................................................................... 47 v LIST OF FIGURES Figure 1-1. Pictoral representation of stylopod (orange), zeugopod (green), and autopod (blue). The autopod is further divided into the mesopodium (the carpals/tarsals) and the acropodium (metacarpals/metatarsals and phalanges). If this were a derived tetrapod forelimb, the orange stylopod would represent the humerus, the green zeugopod would be the radius and ulna, and the blue autopod represents the carpal bones, metacarpals, and phalanges. .................................................................................. 4 Figure 1-2. A µCT image of a mouse wrist (left) demonstrating an elongate pisiform and a histological image of growth plate (right). The pisiform is highlighted in blue in the µCT image. In the histological image the progression from cartilage to bone occurs from the top of this image towards the bottom. .................................................... 7 Figure 2-1 µCT image of newt forelimb generate using Avizo 8.0.1. This scan demonstrates the lack of secondary ossification centers present within the species and furthermore the lack of a pisiform ............................................................................. 18 Figure 2-2. µCT and histological imaging of the 15.25 inches long alligator. Note the lack of epiphyseal development in the µCT image. In this histological image of the alligator pisiform, Safranin O stains cartilages red and Fast Green stains bone and other tissues green. The histological image indicate cartilage with directional growth. ............................................................................................................................. 20 Figure 2-3. µCT image of 48-inch alligator forelimb, indicating a epiphyseal line on the long bone and a lack thereof on the pisiform, further supporting our findings from the 15.25 inch alligator. Red arrow indicates pisiform, blue arrow indicates epiphyseal line. ................................................................................................................. 20 Figure 2-4. µCT and histological analysis of the fence lizard. Staining utilized a modified Periodic Acid Schiff protocol. Note the distinct epiphyseal lines on the µCT image of this juvenile in contrast with the distinct lack of an epiphyseal line within the pisiform. The red arrow indicates the pisiform and the blue arrow indicates an epiphyseal line, here highlighted on the ulna. .................................................................. 22 Figure 2-5. µCT scan of anoles lizard and Periodic Acid Schiff staining of histological section. Like the fence lizard, there are distinct growth plate lines along the long bones of the anoles lizard autopodium and a lack of a secondary ossification center in the pisiform. ................................................................................................................. 22 Figure 2-6. Image data from mouse demonstrating an elongate, rod-like pisiform with a clear secondary center of ossification, as well as a histologically clear growth plate. Compare with images from chapter 1, also featuring a mouse autopod and pisiform growth plate, for review
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