Plasticity Through Canalization: The Contrasting Effect of Temperature on Trait Size and Growth in Drosophila

McDonald, Jeanne M. C.; Ghosh, Shampa M.; Gascoigne, Samuel J L; Shingleton, Alexander W.

doi:10.3389/fcell.2018.00156

Cited by 32 publications

(29 citation statements)

References 34 publications

(61 reference statements)

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“…Each environmental variable (temperature vs. nutrition, for example) can induce independent effects on allometric relationships. Although changes in nutritional conditions proportionally change both adult leg size and wing size, changes in temperature much more strongly affect wing size than leg size ( Azevedo et al 2002 ; Shingleton et al 2009 ; McDonald et al 2018 ). The molecular mechanisms underlying differential sensitivity to environmental stimuli are not clear, but temperature-driven plasticity is, at least partially, regulated in an organ-specific manner via the regulation of cell proliferation ( Azevedo et al 2002 ; Shingleton et al 2009 ; McDonald et al 2018 ).…”

Section: Body-size Controlmentioning

confidence: 99%

“…Although changes in nutritional conditions proportionally change both adult leg size and wing size, changes in temperature much more strongly affect wing size than leg size ( Azevedo et al 2002 ; Shingleton et al 2009 ; McDonald et al 2018 ). The molecular mechanisms underlying differential sensitivity to environmental stimuli are not clear, but temperature-driven plasticity is, at least partially, regulated in an organ-specific manner via the regulation of cell proliferation ( Azevedo et al 2002 ; Shingleton et al 2009 ; McDonald et al 2018 ). Because the molecular mechanism underlying temperature-dependent scaling appears to differ from the ones mediating nutrition-dependent proportionality, which include the insulin/TOR pathway, one might speculate that temperature-sensitive scaling relationships could involve distinct molecular pathways, such as the TGF-β signaling pathway.…”

Section: Body-size Controlmentioning

confidence: 99%

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Regulation of Body Size and Growth Control

Texada¹,

Kaburagi²,

Rewitz³

2020

Genetics

105

146

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The control of body and organ growth is essential for the development of adults with proper size and proportions, which is important for survival and reproduction. In animals, adult body size is determined by the rate and duration of juvenile growth, which are influenced by the environment. In nutrient-scarce environments in which more time is needed for growth, the juvenile growth period can be extended by delaying maturation, whereas juvenile development is rapidly completed in nutrient-rich conditions. This flexibility requires the integration of environmental cues with developmental signals that govern internal checkpoints to ensure that maturation does not begin until sufficient tissue growth has occurred to reach a proper adult size. The Target of Rapamycin (TOR) pathway is the primary cell-autonomous nutrient sensor, while circulating hormones such as steroids and insulin-like growth factors are the main systemic regulators of growth and maturation in animals. We discuss recent findings in Drosophila melanogaster showing that cell-autonomous environment and growth-sensing mechanisms, involving TOR and other growth-regulatory pathways, that converge on insulin and steroid relay centers are responsible for adjusting systemic growth, and development, in response to external and internal conditions. In addition to this, proper organ growth is also monitored and coordinated with whole-body growth and the timing of maturation through modulation of steroid signaling. This coordination involves interorgan communication mediated by Drosophila insulin-like peptide 8 in response to tissue growth status. Together, these multiple nutritional and developmental cues feed into neuroendocrine hubs controlling insulin and steroid signaling, serving as checkpoints at which developmental progression toward maturation can be delayed. This review focuses on these mechanisms by which external and internal conditions can modulate developmental growth and ensure proper adult body size, and highlights the conserved architecture of this system, which has made Drosophila a prime model for understanding the coordination of growth and maturation in animals.

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Section: Body-size Controlmentioning

confidence: 99%

Section: Body-size Controlmentioning

confidence: 99%

Regulation of Body Size and Growth Control

Texada¹,

Kaburagi²,

Rewitz³

2020

Genetics

105

146

View full text Add to dashboard Cite

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“…plasticity in body vs . cell size, which differed across D. melanogaster ’s organs, was shown by McDonald et al (2018). In a study in which different life stages of D. melanogaster were exposed to hypoxia, the cell size response was found to be stage-specific (Heinrich et al, 2011).…”

Section: Discussionmentioning

confidence: 99%

Aerobic scope does matter in temperature-size rule, but only under optimal conditions

Walczyńska

Łabęcka

Sobczyk

2020

Preprint

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3 1 exposure to hypoxia, (iii) this response enables us to keep the wide scope for aerobic 3 2 performance, and (iv) it prevents the decrease in fitness. We conducted our tests on three clones 3 3 of the rotifer Lecane inermis with different thermal preferences. These clones were exposed to 3 4 three experimental regimes: mild hypoxia, severe hypoxia driven by a too high temperature, and 3 5 severe hypoxia driven by an inadequate oxygen concentration. The results showed that our 3 6 causative reasoning was generally correct, but only under mildly hypoxic conditions. In more 3 7 stressful environments, rotifers had clone-and condition-specific responses, which in fact were 3 8 equally successful in terms of the levels of fitness. Our results join for the first time all factors 3 9 connecting the cause and effect in the temperature-size rule. They indicate the importance of the 4 0conditions under which it should be tested. The most important messages from this study was that 4 1 (i) a decrease in the body size was one of but not the only option for preventing fitness reduction 4 2 under hypoxia, and (ii) such a response to higher temperature fuelled the aerobic scope in clone-4 3 specific, thermally optimal conditions. 4 4 4 5 4 6 4 7 4 8 4 9 7 1 2018; Verberk and Atkinson, 2013) and directly (Czarnoleski et al., 2015; Frazier et al., 2001; 7 2 Hoefnagel and Verberk, 2015). However, results relating this pattern directly to organismal 7 3 fitness are scarce (Prokosch et al., 2019; Walczyńska et al., 2015a), while such a reference is the 7 4only way that enables reliable conclusions on the evolutionary meaning of TSR. 7 5In this study, we linked the hypothesized proximate and ultimate mechanisms behind the 7 6 phenotypically driven size decrease with increasing temperature for the case of the rotifer Lecane 7 7inermis. We aimed to thoroughly test the logic of the reasoning behind hypoxia driving body size 7 8shrinkage to prevent the reduction in fitness. Because the TSR has been empirically confirmed to 7 9 be condition-sensitive and to be performed only in an optimal thermal range (Walczyńska et al., 8 0 4 2016), we conducted our tests under optimal and suboptimal conditions; the latter was further 8 1 diversified between hypoxia driven by stress-inducing high temperatures or by the stress-8 2 inducing low oxygen levels. This distinction enabled inference on the possible border conditions 8 3 for TSR performance, linking the hypothesized proximate and ultimate factors with fitness. 8 4We examined the aerobic scope, our hypothesized ultimate mechanism, by estimating the specific 8 5 dynamic action (SDA). This measure refers to the increasing metabolic expenditures in animals 8 6 and is associated with ingestion, digestion, assimilation and absorption of food (McCue, 2006; 8 7 Secor, 2009), when the increasing oxygen consumption was mostly associated with the 8 8 biochemical transformation of food and the synthesis of the new proteins (Jordan and Steffensen, 8 92007). In practice, it was estimated as a difference in...

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“…In D. melanogaster, rearing larvae at lower temperatures also reduces wing growth rates, albeit to a lesser degree than poor nutrition, and extends developmental time. However, in this case even though growth rates are slower, the extended developmental period results in adults with larger wings (McDonald et al, 2018). These findings illustrate that if we want to understand how organs achieve either plasticity or robustness in their final size, we first need to understand how these properties of organ growth change across environmental conditions.…”

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confidence: 88%

Maintaining robust size across environmental conditions through plastic brain growth dynamics

Cobham

Neumann

Mirth

2020

Preprint

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Organ growth is tightly regulated across environmental conditions to generate appropriate final size. While the size of some organs is free to vary, others need to maintain constant size to function properly. This poses a unique problem: how is robust final size achieved when environmental conditions alter the rates and the duration of growth? Brain growth is known to be “spared” from the effects of the environment from humans to fruit flies. Here, we explore how this robustness in brain size is achieved by examining differences in growth dynamics between the larval body, the brain, and the mushroom bodies – a brain compartment – in Drosophila melanogaster across thermal and nutritional conditions. We identify key differences in patterns of growth between the whole brain and mushroom bodies, as well as differences in the signalling pathways implicated, that are likely to underlie robustness of final organ shape. Further, we show that these differences produce distinct brain shapes across environments.

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Plasticity Through Canalization: The Contrasting Effect of Temperature on Trait Size and Growth in Drosophila

Cited by 32 publications

References 34 publications

Regulation of Body Size and Growth Control

Regulation of Body Size and Growth Control

Aerobic scope does matter in temperature-size rule, but only under optimal conditions

Maintaining robust size across environmental conditions through plastic brain growth dynamics

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