skip to main content

Title: The steroid hormone ecdysone regulates growth rate in response to oxygen availability
Abstract In almost all animals, physiologically low oxygen (hypoxia) during development slows growth and reduces adult body size. The developmental mechanisms that determine growth under hypoxic conditions are, however, poorly understood. Here we show that the growth and body size response to moderate hypoxia (10% O 2 ) in Drosophila melanogaster is systemically regulated via the steroid hormone ecdysone. Hypoxia increases level of circulating ecdysone and inhibition of ecdysone synthesis ameliorates the negative effect of low oxygen on growth. We also show that the effect of ecdysone on growth under hypoxia is through suppression of the insulin/IGF-signaling pathway, via increased expression of the insulin-binding protein Imp-L2 . These data indicate that growth suppression in hypoxic Drosophila larvae is accomplished by a systemic endocrine mechanism that overlaps with the mechanism that slows growth at low nutrition. This suggests the existence of growth-regulatory mechanisms that respond to general environmental perturbation rather than individual environmental factors.  more » « less
Award ID(s):
Author(s) / Creator(s):
; ; ; ;
Date Published:
Journal Name:
Scientific Reports
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Animals develop in unpredictable, variable environments. In response to environmental change, some aspects of development adjust to generate plastic phenotypes. Other aspects of development, however, are buffered against environmental change to produce robust phenotypes. How organ development is coordinated to accommodate both plastic and robust developmental responses is poorly understood. Here, we demonstrate that the steroid hormone ecdysone coordinates both plasticity of organ size and robustness of organ pattern in the developing wings of the fruit fly Drosophila melanogaster . Using fed and starved larvae that lack prothoracic glands, which synthesize ecdysone, we show that nutrition regulates growth both via ecdysone and via an ecdysone-independent mechanism, while nutrition regulates patterning only via ecdysone. We then demonstrate that growth shows a graded response to ecdysone concentration, while patterning shows a threshold response. Collectively, these data support a model where nutritionally regulated ecdysone fluctuations confer plasticity by regulating disc growth in response to basal ecdysone levels and confer robustness by initiating patterning only once ecdysone peaks exceed a threshold concentration. This could represent a generalizable mechanism through which hormones coordinate plastic growth with robust patterning in the face of environmental change. 
    more » « less
  2. null (Ed.)
    Abstract Coastal ecosystems experience substantial natural fluctuations in p CO 2 and dissolved oxygen (DO) conditions on diel, tidal, seasonal and interannual timescales. Rising carbon dioxide emissions and anthropogenic nutrient input are expected to increase these p CO 2 and DO cycles in severity and duration of acidification and hypoxia. How coastal marine organisms respond to natural p CO 2  × DO variability and future climate change remains largely unknown. Here, we assess the impact of static and cycling p CO 2  × DO conditions of various magnitudes and frequencies on early life survival and growth of an important coastal forage fish, Menidia menidia . Static low DO conditions severely decreased embryo survival, larval survival, time to 50% hatch, size at hatch and post-larval growth rates. Static elevated p CO 2 did not affect most response traits, however, a synergistic negative effect did occur on embryo survival under hypoxic conditions (3.0 mg L −1 ). Cycling p CO 2  × DO, however, reduced these negative effects of static conditions on all response traits with the magnitude of fluctuations influencing the extent of this reduction. This indicates that fluctuations in p CO 2 and DO may benefit coastal organisms by providing periodic physiological refuge from stressful conditions, which could promote species adaptability to climate change. 
    more » « less
  3. The Steptoean Positive Carbon Isotope Excursion (SPICE) event at ca. 497−494 Ma was a major carbon-cycle perturbation of the late Cambrian that coincided with rapid diversity changes among trilobites. Several scenarios (e.g., climatic/oceanic cooling and seawater anoxia) have been proposed to account for an extinction of trilobites at the onset of SPICE, but the exact mechanism remains unclear. Here, we present a chemostratigraphic study of carbonate carbon and carbonate-associated sulfate sulfur isotopes (δ13Ccarb and δ34SCAS) and elemental redox proxies (UEF, MoEF, and Corg/P), augmented by secular trilobite diversity data, from both upper slope (Wangcun) and lower slope (Duibian) successions from the Jiangnan Slope, South China, spanning the Drumian to lower Jiangshanian. Redox data indicate locally/regionally well-oxygenated conditions throughout the SPICE event in both study sections except for low-oxygen (hypoxic) conditions within the rising limb of the SPICE (early-middle Paibian) at Duibian. As in coeval sections globally, the reported δ13Ccarb and δ34SCAS profiles exhibit first-order coupling throughout the SPICE event, reflecting co-burial of organic matter and pyrite controlled by globally integrated marine productivity, organic preservation rates, and shelf hypoxia. Increasing δ34SCAS in the “Early SPICE” interval (late Guzhangian) suggests that significant environmental change (e.g., global-oceanic hypoxia) was under way before the global carbon cycle was markedly affected. Assessment of trilobite range data within a high-resolution biostratigraphic framework for the middle-late Cambrian facilitated re-evaluation of the relationship of the SPICE to contemporaneous biodiversity changes. Trilobite diversity in South China declined during the Early SPICE (corresponding to the End-Marjuman Biomere Extinction, or EMBE, of Laurentia) and at the termination of the SPICE (corresponding to the End-Steptoean Biomere Extinction, or ESBE, of Laurentia), consistent with biotic patterns from other cratons. We infer that oxygen minimum zone and/or shelf hypoxia expanded as a result of locally enhanced productivity due to intensified upwelling following climatic cooling, and that expanded hypoxia played a major role in the EMBE at the onset of SPICE. During the SPICE event, global-ocean ventilation promoted marine biotic recovery, but termination of SPICE-related cooling in the late Paibian may have reduced global-ocean circulation, triggering further redox changes that precipitated the ESBE. Major changes in both marine environmental conditions and trilobite diversity during the late Guzhangian demonstrate that the SPICE event began earlier than the Guzhangian-Paibian boundary, as previously proposed. 
    more » « less
  4. Abstract

    Males of the Asian rhinoceros beetle, Trypoxylus dichotomus, possess exaggerated head and thoracic horns that scale dramatically out of proportion to body size. While RNAi-mediated knockdowns of the insulin receptor suggest that the insulin signaling pathway regulates nutrition-dependent growth including exaggerated horns, the genes that regulate disproportionate growth have yet to be identified. We used RNAi-mediated knockdown of several genes to investigate their potential role in growth and scaling of the sexually dimorphic, exaggerated head horns of T. dichotomus. Knockdown of the insulin signaling substrate chico and the ecdysone response element broad caused significant decreases in head horn length, while having no or minimal effects on other structures such as elytra and tibiae. However, scaling of horns to body size was not affected by either knockdown. In addition, knockdown of phosphatase and tensin homolog, a negative regulator of the insulin signaling pathway, had no significant effects on any trait. Our results do not identify any candidate genes that may specifically mediate the allometric aspect of horn growth, but they do confirm the insulin signaling pathway as a mediator of conditional trait expression, and importantly implicate the ecdysone signaling pathway, possibly in conjunction with insulin signaling, as an additional mediator of horn growth.

    more » « less
  5. Deoxygenation worldwide is increasing in aquatic systems with implications for organisms' biology, communities and ecosystems. Eastern Baltic cod has experienced a strong decline in mean body condition (i.e. weight at a specific length) over the past 20 years with effects on the fishery relying on this resource. The decrease in cod condition has been tentatively linked in the literature to increased hypoxic areas potentially affecting habitat range, but also to benthic prey and/or cod physiology directly. To date, no studies have been performed to test these mechanisms. Using otolith trace element microchemistry and hypoxia-responding metrics based on manganese (Mn) and magnesium (Mg), we investigated the relationship between fish body condition at capture and exposure to hypoxia. Cod individuals collected after 2000 with low body condition had a higher level of Mn/Mg in the last year of life, indicating higher exposure to hypoxic waters than cod with high body condition. Moreover, lifetime exposure to hypoxia was even more strongly correlated to body condition, suggesting that condition may reflect long-term hypoxia status. These results were irrespective of fish age or sex. This implies that as Baltic cod visit poor-oxygen waters, perhaps searching for benthic food, they compromise their own performance. This study specifically sheds light on the mechanisms leading to the low condition of cod and generally points to the impact of deoxygenation on ecosystems and fisheries. 
    more » « less