Browsing by Author "Shingleton, Alexander W."
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- Coordination of Wing and Whole-Body Development at Developmental Milestones Ensures Robustness against Environmental and Physiological PerturbationsPublication . Oliveira, Marisa M.; Shingleton, Alexander W.; Mirth, Christen K.Development produces correctly patterned tissues under a wide range of conditions that alter the rate of development in the whole body. We propose two hypotheses through which tissue patterning could be coordinated with whole-body development to generate this robustness. Our first hypothesis states that tissue patterning is tightly coordinated with whole-body development over time. The second hypothesis is that tissue patterning aligns at developmental milestones. To distinguish between our two hypotheses, we developed a staging scheme for the wing imaginal discs of Drosophila larvae using the expression of canonical patterning genes, linking our scheme to three whole-body developmental events: moulting, larval wandering and pupariation. We used our scheme to explore how the progression of pattern changes when developmental time is altered either by changing temperature or by altering the timing of hormone synthesis that drives developmental progression. We found the expression pattern in the wing disc always aligned at moulting and pupariation, indicating that these key developmental events represent milestones. Between these milestones, the progression of pattern showed greater variability in response to changes in temperature and alterations in physiology. Furthermore, our data showed that discs from wandering larvae showed greater variability in patterning stage. Thus for wing disc patterning, wandering does not appear to be a developmental milestone. Our findings reveal that tissue patterning remains robust against environmental and physiological perturbations by aligning at developmental milestones. Furthermore, our work provides an important glimpse into how the development of individual tissues is coordinated with the body as a whole.
- Ecdysone promotes growth of imaginal discs through the regulation of Thor in D. melanogasterPublication . Herboso, Leire; Oliveira, Marisa M.; Talamillo, Ana; Pérez, Coralia; González, Monika; Martín, David; Sutherland, James D.; Shingleton, Alexander W.; Mirth, Christen K.; Barrio, RosaAnimals have a determined species-specific body size that results from the combined action of hormones and signaling pathways regulating growth rate and duration. In Drosophila, the steroid hormone ecdysone controls developmental transitions, thereby regulating the duration of the growth period. Here we show that ecdysone promotes the growth of imaginal discs in mid-third instar larvae, since imaginal discs from larvae with reduced or no ecdysone synthesis are smaller than wild type due to smaller and fewer cells. We show that insulin-like peptides are produced and secreted normally in larvae with reduced ecdysone synthesis, and upstream components of insulin/insulin-like signaling are activated in their discs. Instead, ecdysone appears to regulate the growth of imaginal discs via Thor/4E-BP, a negative growth regulator downstream of the insulin/insulin-like growth factor/Tor pathways. Discs from larvae with reduced ecdysone synthesis have elevated levels of Thor, while mutations in Thor partially rescue their growth. The regulation of organ growth by ecdysone is evolutionarily conserved in hemimetabolous insects, as shown by our results obtained using Blattella germanica. In summary, our data provide new insights into the relationship between components of the insulin/insulin-like/Tor and ecdysone pathways in the control of organ growth.
- Integrating Body and Organ Size in Drosophila: Recent Advances and Outstanding ProblemsPublication . Mirth, Christen Kerry; Shingleton, Alexander W.OVER THE PAST TWO DECADES, FUNDAMENTAL STRIDES IN PHYSIOLOGY AND GENETICS HAVE ALLOWED US TO FINALLY GRASP THE DEVELOPMENTAL MECHANISMS REGULATING BODY SIZE, PRIMARILY IN ONE MODEL ORGANISM: the fruit fly Drosophila melanogaster. In Drosophila, as in all animals, final body size is regulated by the rate and duration of growth. These studies have identified important roles for the insulin and the target of rapamycin (TOR) signaling pathways in regulating the growth rate of the larva, the stage most important in determining final adult size. Furthermore, they have shown that the insulin/TOR pathway interacts with hormonal systems, like ecdysone and juvenile hormone, to regulate the timing of development and hence the duration of growth. This interaction allows the growing larvae to integrate cues from the environment with environmentally sensitive developmental windows to ensure that optimal size and proportions are reached given the larval rearing conditions. Results from this work have opened up new avenues of studies, including how environmental cues are integrated to regulate developmental time and how organs maintain proportional growth. Other researchers interested in the evolution of body size are beginning to apply these results to studies of body size evolution and the generation of allometry. With these new findings, and with the developments to come, the field of size control finds itself in the fortunate position of finally being able to tackle century old questions of how organisms achieve final adult size and proportions. This review discusses the state of the art of size control from a Drosophila perspective, and outlines an approach to resolving outstanding issues.
- The developmental control of size in insectsPublication . Nijhout, H. Frederik; Riddiford, Lynn M.; Mirth, Christen; Shingleton, Alexander W.; Suzuki, Yuichiro; Callier, VivianeThe mechanisms that control the sizes of a body and its many parts remain among the great puzzles in developmental biology. Why do animals grow to a species-specific body size, and how is the relative growth of their body parts controlled to so they grow to the right size, and in the correct proportion with body size, giving an animal its species-characteristic shape? Control of size must involve mechanisms that somehow assess some aspect of size and are upstream of mechanisms that regulate growth. These mechanisms are now beginning to be understood in the insects, in particular in Manduca sexta and Drosophila melanogaster. The control of size requires control of the rate of growth and control of the cessation of growth. Growth is controlled by genetic and environmental factors. Insulin and ecdysone, their receptors, and intracellular signaling pathways are the principal genetic regulators of growth. The secretion of these growth hormones, in turn, is controlled by complex interactions of other endocrine and molecular mechanisms, by environmental factors such as nutrition, and by the physiological mechanisms that sense body size. Although the general mechanisms of growth regulation appear to be widely shared, the mechanisms that regulate final size can be quite diverse.
- The sex-specific effects of diet quality versus quantity on morphology in Drosophila melanogasterPublication . Shingleton, Alexander W.; Masandika, Josephine R.; Thorsen, Lily S.; Zhu, Yuqing; Mirth, Christen K.Variation in the quality and quantity of nutrition is a major contributor to phenotypic variation in animal populations. Although we know much of how dietary restriction impacts phenotype, and of the molecular-genetic and physiological mechanisms that underlie this response, we know much less of the effects of dietary imbalance. Specifically, although dietary imbalance and restriction both reduce overall body size, it is unclear whether both have the same effect on the size of individual traits. Here, we use the fruit fly Drosophila melanogaster to explore the effect of dietary food versus protein-to-carbohydrate ratio on body proportion and trait size. Our results indicate that body proportion and trait size respond differently to changes in diet quantity (food concentration) versus diet quality (protein-to-carbohydrate ratio), and that these effects are sex specific. While these differences suggest that Drosophila use at least partially distinct developmental mechanisms to respond to diet quality versus quantity, further analysis indicates that the responses can be largely explained by the independent and contrasting effects of protein and carbohydrate concentration on trait size. Our data highlight the importance of considering macronutrient composition when elucidating the effect of nutrition on trait size, at the levels of both morphology and developmental physiology.