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16. Epigenetic Integration, Complexity, and Evolvability of the Head: Rethinking the Functional Matrix Hypothesis
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271 Epigenetics: Linking Genotype and Phenotype in Development and Evolution, ed. Benedikt Hallgrímsson and Brian K. Hall. Copyright by The Regents of the University of California. All rights of reproduction in any form reserved. 16 epigenetic Integration, complexity, and evolvability of the Head RETHINKING THE FUNCTIONAL MATRIX HYPOTHESIS Daniel E. lieberman As I get older, I find myself increasingly hesitant to use the word epigenetics because I worry about employing a term that is so liable to engender confusion and disagreement. Many biologists define epigenetics in a narrow sense solely as heritable changes in the phenotype that derive from molecular mechanisms other than sequence changes in the genotype (the classic example being methylation). However, Waddington, who coined the word in 1942, and other early users of the term had a broader concept in mind, one that captured the variable effects of interactions between genes, embryonic development, and the environment. According to this original and more encompassing definition, epigenetics refers to the vast set of processes by which alternative, variable phenotypes––cellular, anatomical, physiological , even behavioral––derive from a given genotype (see Haig, 2004). Not surprisingly, there is a rich literature on epigenetics in complex organisms because many layers and types of epigenetic interactions are essential to initiate the development and integration of diverse units so that they grow and function together appropriately (Wagner, 2001; Kirschner and Gerhart, 2005; West-Eberhard, 2003). Epigenetic interactions occur at each hierarchical level of development including within the genome; among cells, tissues, and organs; and between an organism and its environment. conTenTs Epigenetic Integration During Craniofacial Development Patterning Morphogenesis Growth The Functional Matrix Hypothesis Revisited Applying the Model (Brain Size in Human Evolution) References 272 epigenetics in evolution and disease Epigenetic interactions play major roles in the development and evolution of every complex phenotype, but vertebrate heads are an extreme case that merits particular consideration because of their special complexity, both structurally and functionally. Structurally, heads are complex because they comprise an astonishing array of diverse tissues and organs in a comparatively small, restricted space. In a typical adult human, these structures include 22 bones that derive from hundreds of ossification centers, 32 teeth, many dozens of muscles, the brain (itself comprised of many major units), eyes, olfactory bulbs, the organs of balance, the organs of hearing , the pharynx, various glands, as well as the many nerves, veins, arteries, and sinuses that supply, drain, and innervate these structures. Functionally, the head participates in a wide array of tasks including perception, cognition, memory, vision, taste, olfaction, hearing, balance , chewing, swallowing, vocalization, respiration , and thermoregulation. How could such a degree of complexity and multifunctionality develop, let alone evolve, without massive levels of epigenetic interactions? A thought experiment may help to illustrate this point. Imagine you are an engineer and have been given the task of creating a robotic head of human size that carries out the same functions as a human head and with similar levels of performance. To complicate matters further , the robotic head needs not only to perform all these functions effectively under many circumstances (extreme heat, cold, dryness, wetness , when upside-down, etc.) but also to be able to grow from the size of a walnut to that of a soccer ball without any compromise in function . Needless to say, you would probably quit your job or go mad because this kind of engineering is currently impossible, even unimaginable . Yet, evolution has managed this feat effectively and with many different models. Over countless generations, natural selection has operated more like a tinker than an engineer, using a wide range of heritable and available components in novel ways to create heads that function superbly in a wide range of demanding tasks, grow manyfold in size, and even look attractive in many cases. The complexity of the head, both structurally and functionally, raises a paradox. From an engineering standpoint, one might imagine that very complex and functionally vital parts of the body like the head are tightly constrained. Any change, such as a larger brain or smaller canines , would presumably disrupt how the head grows and functions, leading to a loss of integration and, hence, a decline in performance. In a world full of competitors and predators, natural selection would eliminate any variant that could not see, smell, chew, or hear as well as its competitors. Yet, heads are actually very evolvable (capable of generating a wide range of heritable, phenotypic variation), as is evident from the extraordinary diversity of mammalian skulls in terms of...