Abstract
Heterochrony is an enabling concept in evolution theory that metaphorically captures the mechanism of biologic change due to mechanisms of growth and development. The spatio-temporal patterns of morphogenesis are determined by cell-to-cell signaling mediated by specific soluble growth factors and their cognate receptors on nearby cells of different germline origins. Subsequently, down-stream production of second messengers generates patterns of form and function. Environmental upheavals such as Romer’s hypothesized drying up of bodies of water globally caused the vertebrate water-land transition. That transition caused physiologic stress, modifying cell-cell signaling to generate terrestrial adaptations of the skeleton, lung, skin, kidney and brain. These tissue-specific remodeling events occurred as a result of the duplication of the Parathyroid Hormone-related Protein Receptor (PTHrPR) gene, expressed in mesodermal fibroblasts in close proximity to ubiquitously expressed endodermal PTHrP, amplifying this signaling pathway. Examples of how and why PTHrPR amplification affected the ontogeny, phylogeny, physiology and pathophysiology of the lung are used to substantiate and further our understanding through insights to the heterochronic mechanisms of evolution, such as the fish swim bladder evolving into the vertebrate lung, interrelated by such functional homologies as surfactant and mechanotransduction. Instead of the conventional description of this phenomenon, lung evolution can now be understood as adaptive changes in the cellular-molecular signaling mechanisms underlying its ontogeny and phylogeny.
Highlights
Heterochrony is an enabling concept in evolution theory because it captures the image of dynamic biologic change diachronically across space and time
Developmental Biology [5] beginning in the late 1970s with the discovery of soluble growth factors and their complementary receptors residing on neighboring cell-types, determining the patterns of morphogenesis [6]
In the case of the lung, it facilitated the formation of alveoli [28]; in the kidney, PTHrP signaling amplification generated glomeruli [29]; in bone, increased PTHrP amplification allowed for the five documented phenotypic changes in the skeleton that compensated for the increased effect of gravity on the skeleton relative to buoyancy in water [30]; in the skin, PTHrP fostered barrier formation by skin cells for prevention of water and electrolyte loss [31]; the brain is thought to have evolved from the skin [32], and it has a number of molecular traits that are derivative of the latter at the molecular level [9] that would have facilitated its evolution for land adaptation
Summary
Heterochrony is an enabling concept in evolution theory because it captures the image of dynamic biologic change diachronically across space and time. The current article demonstrates the value added in understanding heterochrony as a sequence of cell-cell interactions that can be modified by environmental factors to understand how and why evolution has occurred The power of this approach is in its ability to understand the processes of development, physiology, homeostasis and pathology as one continuous, scale free evolutionary mechanism for the first time. This is an iterative process by which the zygote divides, giving rise to the animal and vegetal poles, the blastula, gastrula, and so on [17] during embryogenesis, followed by fetal growth and differentiation [18] to generate the offspring All of these processes are mediated by growth factor-receptor signaling mechanisms that form the tissues and organs of the body. In the case of the lung, it facilitated the formation of alveoli [28]; in the kidney, PTHrP signaling amplification generated glomeruli [29]; in bone, increased PTHrP amplification allowed for the five documented phenotypic changes in the skeleton that compensated for the increased effect of gravity on the skeleton relative to buoyancy in water [30]; in the skin, PTHrP fostered barrier formation by skin cells for prevention of water and electrolyte loss [31]; the brain is thought to have evolved from the skin [32], and it has a number of molecular traits that are derivative of the latter at the molecular level [9] that would have facilitated its evolution for land adaptation
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