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WIREs Dev Biol
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Network‐regulated organ allometry: The developmental regulation of morphological scaling

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Abstract Morphological scaling relationships, or allometries, describe how traits grow coordinately and covary among individuals in a population. The developmental regulation of scaling is essential to generate correctly proportioned adults across a range of body sizes, while the mis‐regulation of scaling may result in congenital birth defects. Research over several decades has identified the developmental mechanisms that regulate the size of individual traits. Nevertheless, we still have poor understanding of how these mechanisms work together to generate correlated size variation among traits in response to environmental and genetic variation. Conceptually, morphological scaling can be generated by size‐regulatory factors that act directly on multiple growing traits (trait‐autonomous scaling), or indirectly via hormones produced by central endocrine organs (systemically regulated scaling), and there are a number of well‐established examples of such mechanisms. There is much less evidence, however, that genetic and environmental variation actually acts on these mechanisms to generate morphological scaling in natural populations. More recent studies indicate that growing organs can themselves regulate the growth of other organs in the body. This suggests that covariation in trait size can be generated by network‐regulated scaling mechanisms that respond to changes in the growth of individual traits. Testing this hypothesis, and one of the main challenges of understanding morphological scaling, requires connecting mechanisms elucidated in the laboratory with patterns of scaling observed in the natural world. This article is categorized under: Establishment of Spatial and Temporal Patterns > Regulation of Size, Proportion, and Timing Comparative Development and Evolution > Organ System Comparisons Between Species
Scaling relationships among organs and other traits capture the shape of an organism and how that shape changes with body size. The scaling relationship is described by the linear equation log TB = α log TA + log b. If the slope of the line, α, is 1, body proportion is constant across a range of body sizes, referred to as isometric scaling. An increase (long dash line) or decrease (short dash line) in the slope reflects a disproportionate increase or decrease in the relative size of a trait with an overall increase in size, referred to as hyper‐ or hypoallometric scaling respectively. A change in intercept, log b, (grey line) results in a proportional increase in relative trait size across the full range of body sizes
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Changing the slope of morphological scaling relationships. (a) Morphological scaling arises because traits (TA and TB) share a correlated response to variation in an environmental or genetic regulator of size (V). If traits have the same sensitivity to variation in the size regulator, they will scale isometrically to each other. (b) If one trait (TB) is more sensitive than the other trait (TA) to the size regulator, then TB will scale hyperallometrically to TA when size varies in response to variation in the size regulator. If TB is less sensitive than TA to the size regulator, TB will scale hypoallometrically to TA (not shown)
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Organ‐autonomous size regulation and network‐regulated scaling. (a) Models of organ‐autonomous size regulation argue that cell proliferation in imaginal discs is stimulated by a morphogen gradients (blue circle) at the center of the disc and the effect of mechanical force generating stretch (tension) at the periphery of the disc (black arrows). (b) Growth stops due to compression on the cells at the center of the disc (black arrows), which reduces stretch at the periphery of the disc (grey arrows) stopping growth there also. (c) In Drosophila melanogaster discs are able to signal their growth status to the rest of the body by releasing dILP8 and DPP which either indirectly or directly regulate the synthesis of ecdysone. Growth perturbation of one disc suppresses ecdysone synthesis and slows growth of discs across the body in a tightly coordinated manner
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Development control systems that generate morphological scaling through the regulation of growth rate. (a) In humans and other mammals, growth rate is coordinated by circulating IGF1, the release of which is in turn regulated by growth hormone (GH) released by the pituitary gland. Malnutrition has a systemic effect on growth in part by suppressing both the release of GH and reducing the sensitivity of the liver to GH, both of which may reduce levels of circulating IGF1. (b) In Drosophila melanogaster growth of the imaginal discs is coordinated both by circulating insulin‐like peptides (dILPs) and ecdysone, which are regulated by a complex network of signaling from different tissues. Malnutrition has a systemic effect on growth by suppressing the synthesis and/or release of dILPs, and elevating ecdysone levels. See text for more details
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Development control systems that generate morphological scaling through the regulation of developmental time. (a) Variation in nutrition affects the timing of gonadal steroid synthesis, which in turn affects the duration of growth of the long bones in the arms and legs. (b) The relationship between testosterone levels and growth rate in human males, showing that growth stops once testosterone levels reach their peak. (Reprinted with permission from Bozzola, & Meazza, (2011). Copyright Springer and Kelsey et al. (2014), Copyright PLOS.) (c) Variation in nutrition also affects the timing of ecdysone synthesis in Drosophila melanogaster and other holometabolous insects, which in turn affects the duration of body and imaginal disc growth. (d) Attainment of critical size in the third larval instar initiates a hormonal cascade that causes an increase in the level of circulating ecdysone. Growth of the body and imaginal discs stop when ecdysone levels rise above a particular threshold, defining the terminal growth period of the body and discs. (Reprinted with permission from Shingleton (2010), Copyright Landes Bioscience.)
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Developmentally regulated aspects of morphological scaling relationships. The slope, intercept and scatter (tightness) of the scaling relationship can be regulated by changing key aspects of the developmental control system (see Figure 3c–e). TA and TB are Trait A and B respectively, grey lines show scaling where the slope or intercept changed
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Ontogenetic growth patterns and developmental control systems that generate morphological scaling. (a) One pattern of ontogenetic scaling is where one trait (TB) grows after a second trait (TA) has stopped growing. (b) A second pattern of ontogenetic scaling is where both traits (TA and TB) start and stop growing at the same time. (c) A trait‐autonomous scaling mechanism generates covariation in trait size when each trait responds individually, but in a correlated way, to a shared environmental or genetic condition. (d) A systemically regulated scaling mechanism generates covariation in trait size when environmental or genetic factors affect the synthesis and release of a growth‐regulating hormone. (e) A network‐regulated scaling mechanism combines trait‐autonomous and systemically regulated scaling mechanisms, but where individual traits are able to signal their growth status to other traits, either indirectly by regulating the release of growth‐regulating hormones, or directly, by some other signals. TA and TB are growing traits, V is an environmental or genetic growth regulator that varies among individuals, S is a systemic growth‐regulating hormone. Solid arrows are experimentally demonstrated interactions, dotted arrows are putative interactions
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The relationship between ontogenetic (thin grey line), static (black thick line) and evolutionary (thin line) scaling relationships. Ontogenetic scaling describes size covariation among traits in the same individual through time. Static scaling describes size covariation among traits in multiple individuals at the same developmental stage. Evolutionary scaling describes the covariation in mean trait size among different populations or species. (Reprinted with permission from Shingleton and Frankino (2018). Copyright 2018 Elsevier Inc.)
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