Why Muscles Look and Act the Way They Do: Uncovering the Nexus Among Form, Function, Behavior, and Evolution.

Abstract

My two favorite books are Homer Price (and the Doughnut Machine) by McClosky (1943) and De Humani Corporis Fabrica Libri Septem (On the fabric of the human body in seven books) by Vesalius (1543) (my psychiatrist wife says I definitely need therapy; that is, more therapy, if these are my favorites.) At first glance one would not see much common ground between them, but they actually share quite a bit, at least for me. The first captured my imagination in Fifth grade; I love doughnuts, and the thought of a fanciful doughnut machine has never left me. I even thought of going into the doughnut business as a child (maybe still, if funding continues as it is), and I remain fascinated to this day by local doughnut emporiums; I'm riveted to all those near-perfect circles bathed in a cacophony of colors and sprinkled with sweet shavings. Some even harbor inner treasures of crème or custard or chocolate. Indeed, my favorite holiday (I am an equal-faith holiday observer; about 243 a year by my count, which explains my waistline) is the Hebrew Festival of Lights, or Hannukah, in which you are mandated to eat fried foods to celebrate the miracle of the Temple oil lasting for eight days. This has evolved as a quasi-commandment to eat sufganiyah, or jelly-doughnuts (I also interpret the law so as to eat fried chicken.) The second book I did not discover until my graduate school days at Yale. One day, my Advisor, mentor, and surrogate father, Ed Crelin, revered Professor of Anatomy, told me that we were not doing any experiments that day (I was thrilled as nothing had worked for the last week anyway) as he had a rare “treat” in store. I followed him from our lab on the third floor of the Sterling Hall of Medicine to the Harvey Cushing/John Hay Whitney Medical Library some floors below. There we met Dr. Frank Netter, one of the most respected medical illustrators of the 20th century. Netter was working with Dr. Crelin on manuscripts slated for the noted Ciba Clinical Symposia that would portray anatomy and its development via novel perspectives (Crelin, 1975, 1976, 1981). We were going to the Library to gain insights—and inspiration—from some of the great anatomical works that dwelled within. Yale's historical libraries are amongst the greatest in the world, and would become a frequent refuge for me. The historical treasures in the Medical Library boast one of the most complete collections of the works of Vesalius (“Vesaliana”), including an original 1543 edition of his Fabrica. I vividly remember an aged librarian taking us to a small room, bringing in an ornate folio-sized box, which he reverently opened to reveal the Fabrica itself. Before opening the treasure, the librarian peered at me—the look all librarians seem to have for those who are too near their prize children—and asked rather sharply, “Son, have you met an original of the Fabrica before?” “Joe, he's right out of Brooklyn; doubt he's even been to a library.” Dr. Crelin chimed in, sort of joking. “C'mon Joe, let's see the stuff!” (Dr. C was a “cut-to-the-chase” type of fellow; an enigma at Yale, being a senior Professor who wore overall's, string ties, and mopped his own laboratory floor to get it sufficiently clean. They broke the mold with him!) And there it was. The treasure opened, and I was looking at the title page of the most influential writing in the history of medicine, arguably, in all of science. It was a strange, almost surreal feeling, starring at the original page itself. I had, of course, seen pictures of the famous title page before, but never the actual item. I hadn't really “looked” at it before; never felt its warmth before. Now, here in front of me, was Vesalius, seemingly alive, demonstrating the cadaver to the throngs around him, forever shattering the Galenic tradition of “the Professor in the chair,” aloof, detached from students, separated from actual learning, from science. Vesalius’ contribution was to bring students and teachers together; he destroyed an old order, and was not only the bedrock of modern anatomy, but also the stimulant for all subsequent empirical learning in medicine. “Amazing thing about all this,” said Netter in his gruff-sounding tones, “is that we are still not exactly sure who the artists that gave life to this masterpiece were. Most think they were young folks from the Titian School (Saunders and O'Malley, 1950) Others think it was done by van Calcar (Flemish artist Jan Stephen van Calcar). Look, you can see differences and variations throughout…” He went on to explain many specifics that went over my head. Crelin had artistic leanings, so he followed Netter's explanations. I was still stuck in awe at the title page itself, envisioning myself in the crowd looking down upon maestro Vesalius demonstrating the body. Dr. Netter snapped me back to this century: “Jeff, if you think the beginning is something, let's look at the best of the best. May, I?…”—and the greatest medical illustrator of the 20th century turned to the most beautiful, engrossing anatomical art from the 16th century. He opened to the beginning of Book II, the Muscle Men. The illustrations that are now collectively referred to as the “Muscle Men” are the most unforgettable images in all of the Fabrica, perhaps among all images in the history of anatomical drawings. We have all seen them; fluid depictions of men in progressive states of dissection. They stand, or bend, or appear to move, seemingly alive while of course dead. And all of this before the peaceful and serene background landscapes of what is thought to be the Eugenean hills at the outskirts of Venice or, more likely, those near Padua, where Vesalius studied and later taught. I am not an art cognoscenti; I just don't have the gene. I usually won't even enter a museum unless there is a mounted dinosaur within 30 feet of the entrance. But the masterpieces I met that day would not leave my thoughts. We must have stayed for hours, and I hung on every word that my artist/anatomist guides uttered in describing the wonders before us. I could feel the reverence, the adoration, that these accomplished professionals held for the timeless linkages to our past. Before this visit I was a graduate student; after it, an anatomist. I had met my heritage. The stories about doughnuts I so reveled in as young boy, and the magnificence of Vesalius’ portrayal of dissections I met as a graduate student, kindled the same emotions in me: awe and wonder. You do not hear these words used much any longer. Such emotions are rare in today's jaded world in which a flick of a $1,000 iPhone can produce anything/anytime on the Internet. Yet for me, from a far simpler age, my mind was set aflutter from these encounters. Each, in its own way, drew me to ponder about the intersection of form to function, how a structure—be it a perfectly made doughnut or the muscles of the human leg—came to be. Where is that intersection, that holy grail of perfection, where a structure's form is fitted exquisitely to its behavioral activities? Indeed, is there perfection, solely the attempt, or naught but randomness occasionally landing upon some biological kismet? Clearly, minds much sharper than mine have explored such questions, and my remembrances with Vesalian Muscle Men are a perfect segue to some such individuals and this insightful Special Issue of The Anatomical Record aptly titled, “Behavioral Correlates of Muscle Functional Morphology.” This Special Issue is Guest Edited by anatomists/functional morphologists/comparative biologists Adam Hartstone-Rose of North Carolina State University, Damiano Marchi of the University of Pisa, and Sharlene Santana of the University of Washington and the Burke Museum of Natural History and Culture. The Issue will be presented in two volumes, the first, this volume (Hartstone-Rose and Santana, 2018), focusing on cranial muscles, their behavioral correlates and evolutionary trajectories. The second volume will address the world of post-cranial (i.e., limb) muscles. This Special Issue grew out of a Symposium entitled “Muscle functional morphology beyond gross anatomy” held at the 11th International Congress of Vertebrate Morphology in 2016 in Bethesda, Maryland and organized by Drs. Hartsone-Rose and Marchi. These three Guest Editors bring to the fore their individual expertise in muscle biology, Hartstone-Rose and Santana living in the head and neck, largely jaws and mastication, and Marchi marching along among limb muscles. These folks not only bring anatomical diversity to the topics under their collective scalpels and scopes, but also hail from different corners of the globe, adding their own interesting histories and backgrounds. Santana, for example, is a native of Venezuela, where she not only took her undergraduate degree, but where her passion for bats first flew into her heart. Subsequent to that exposure, her interests led Santana to Massachusetts for more bat work, before a stint in California studying facial coloration in primates. Her Co-Guest Editor, Marchi, is a homegrown product of northern Italy. He studies functional morphology of humans and our primate relatives at the University of Pisa, a few hours south and west of Vesalius’ nest at Padova. While I have known of the excellent science of Santana and Marchi from their publications, for full disclosure, I have been aware of Hartstone-Rose's “creativity and genius” since he was a boy. I heard about “little Adam,” first from his brilliant father, David, who was a coworker and a dean at my school for many years (and first Director of our AIDS Center); and from my close friend and world-renown anthropologist and curator of Anthropology at the American Museum of Natural History, Ian Tattersall. Indeed, that's where I first must have met him, as Adam was always there busily making molds and casts of fossil hominids under the tutelage of Ian and Gary Sawyer, the latter, a most creative scientific technician there. The kid even won the top prize at the famous NYC Science Fair (on lemur orbital anatomy) that gave him a full scholarship to NYU (I'm still paying off my geniuses’ college bills!). I heard about Adam again from my former Yale prof, Elwyn Simons, who “stole” him away from NYU and brought him to Duke's famed Lemur Center after Elwyn migrated south from New Haven. I followed Adam's peregrinations—from studying lemur behavior in Madagascar, to taking courses in Australia and Oxford, to completing his PhD (and finally getting a job; poppa was so happy!) at Penn State, then University of South Carolina, and now migrating a bit north to North Carolina State. Who needs the Navy when there are primates and other interesting beasties sprinkled all over the globe to study? Being a native New Yorker, we all expect him home soon. Hartstone-Rose, Santana, and Marchi represent the school of functional/comparative morphologists for whom looking at structure is but step one of the investigation. These scientists are the antithesis of the structural morphologist of years gone by who would assess each bump and lump on a skull and then measure such with calipers in hand and then…stop. While description of the physical world is a start, and a valuable one, it is but the entry portal to the hypothesis. These editors have all had a varied background as morphologists and behaviorists that have shaped the hypotheses they wish to test and the questions they ask. Hartstone-Rose and coworkers assembled a merry band of like-minded, creative researchers for this Special Issue. In this first volume alone, we will encounter those exploring the nexus of cranial muscle functional morphology and questions of cranial shape and paths leading to such in groups ranging from cichlids to rodents, from bats to phalangeriform marsupials to extinct fossil lemurs. And our extant nonhuman primate relatives, long a favorite of this journal (Laitman, 2010), show their smiling (and chewing) faces through many a page in this issue. On the morphological side, approaches and techniques vary to fit the questions, with both traditional dissection and craniometrics to those using model testing to the latest DiceCT and XROMM technology. Some weeks back, I sat down to read a number of these soon to be hatched manuscripts with my coffee in one hand and something called a “cronut” emerging from a gold-covered box in front of me. “What's this?” I asked one of my eternal tax-deductions who did not win a full scholarship to NYU. “Just try it, dad. You might like it. It's a doughnut that has evolved. It's a croissant based relative of your boring, old jelly doughnut. Stop living in the Jurassic; evolve a little!” My reply: “Some things should not evolve. And what is this odd stuff oozing from it?” My offspring's retort was, “It's fig essence. This month's flavor is Fig Caramelia.” “What? There's one flavor a month, and it's fig?!” I stammered. “I just asked you to bring me a few jelly doughnuts. Not some mutant that probably cost a few dollars….” “They are $5.00 each. So EAT IT! You're always babbling about evolution, well, let those evolved teeth of yours combine with your evolved muscles and eat the cronut; welcome to the future!” As this Special Issue on the interface of muscle biology, function, behavior, and evolutionary forces will majestically illustrate, the nexus of shape with form and function is amongst the most fascinating of topics, yet amongst the most difficult to approach. It is this nexus that the scientists within are searching for. Perhaps a question too complex to actually answer, but one the questioners are to be commended for approaching. The journey within this Special Issue is truly fascinating, as it will bring out the extraordinary yin/yang of behavior and evolutionary change. As to the cronut…