Decoupling development and energy flow during embryonic diapause in the cricket,<i>Allonemobius socius</i>

Reynolds, Julie A.; Hand, Steven C.

doi:10.1242/jeb.027359

Cited by 40 publications

(33 citation statements)

References 54 publications

(56 reference statements)

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“…For embryos of the cricket A. socius, the ATP:ADP ratio is approximately 40-50% lower in diapausing versus non-diapausing embryos (Reynolds and Hand, 2009). Likewise, diapausing cysts and embryos from A. franciscana and A. limnaeus contain considerably more ATP than ADP, although the ratio is substantially lower than that measured for post-diapause embryos (Table 1).…”

Section: Mitochondrial Membrane Potential and Proton Leakmentioning

confidence: 78%

“…However, as development proceeds, the metabolism of non-diapause embryos continues to rise along with the increase in cell number per embryo. Accordingly, the aerobic metabolism in 15-day diapausing embryos is only 36% of the rate measured for 15-day non-diapausing embryos, which emphasizes that the ontogenetic increase in metabolism observed in actively developing embryos is blocked during diapause (Reynolds and Hand, 2009).…”

Section: Metabolic Depression During Diapausementioning

confidence: 83%

“…Whether or not downregulation of energy flow occurs depends upon the species and the stage of development in question. For example, in the southern ground cricket, Allonemobius socius, embryonic diapause is not accompanied by a statistically significant change in metabolism (Reynolds and Hand, 2009) when one compares non-diapausing and diapausing embryos at the same developmental stage (Fig. 2).…”

Section: Metabolic Depression During Diapausementioning

confidence: 99%

“…Diapause is a programmed arrest of development that is controlled by endogenous physiological factors and may or may not involve depression of metabolism (Lees, 1955;Tauber and Tauber, 1976;Podrabsky and Hand, 1999;Denlinger, 2002;Reynolds and Hand, 2009;MacRae, 2010;Clegg, 2011;Hahn and Denlinger, 2011;Hand et al, 2011;Patil et al, 2013). Diapause typically precedes the onset of adverse environmental conditions, and production of diapausing embryos is often induced by environmental factors that offer reliable cues for predicting future conditions, such as photoperiod or food quality/availability.…”

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confidence: 99%

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Physiological strategies during animal diapause: lessons from brine shrimp and annual killifish

Podrabsky

Hand

2015

Journal of Experimental Biology

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Diapause is a programmed state of developmental arrest that typically occurs as part of the natural developmental progression of organisms that inhabit seasonal environments. The brine shrimp Artemia franciscana and annual killifish Austrofundulus limnaeus share strikingly similar life histories that include embryonic diapause as a means to synchronize the growth and reproduction phases of their life history to favorable environmental conditions. In both species, respiration rate is severely depressed during diapause and thus alterations in mitochondrial physiology are a key component of the suite of characters associated with cessation of development. Here, we use these two species to illustrate the basic principles of metabolic depression at the physiological and biochemical levels. It is clear that these two species use divergent molecular mechanisms to achieve the same physiological and ecological outcomes. This pattern of convergent physiological strategies supports the importance of biochemical and physiological adaptations to cope with extreme environmental stress and suggests that inferring mechanism from transcriptomics or proteomics or metabolomics alone, without rigorous follow-up at the biochemical and physiological levels, could lead to erroneous conclusions.

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Section: Mitochondrial Membrane Potential and Proton Leakmentioning

confidence: 78%

Section: Metabolic Depression During Diapausementioning

confidence: 83%

Section: Metabolic Depression During Diapausementioning

confidence: 99%

mentioning

confidence: 99%

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Physiological strategies during animal diapause: lessons from brine shrimp and annual killifish

Podrabsky

Hand

2015

Journal of Experimental Biology

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“…In general, diapausing animals survive extended periods of developmental arrest by increasing nutrient stores during diapause preparation, and reducing metabolism during developmental arrest. How these metabolic changes are achieved differs among species: insects vary in the degree that metabolism is suppressed during diapause (Chaplin and Wells, 1982;Denlinger et al, 1972;Reynolds and Hand, 2009a), and in the specific nutrient compositions that are stored and later utilized, although energy stores in form of triacylglycerides (Danks, 1987;Hahn and Denlinger, 2007), glycogen (Danks, 1987;Zhou and Miesfeld, 2009) and specialized storage proteins (Burmester, 1999;Denlinger et al, 2005) are common. Below, we discuss gene expression changes underlying the metabolism of different types of nutrient stores during diapause.…”

Section: The Journal Of Experimental Biology 216 (21)mentioning

confidence: 99%

RNA-Seq reveals early distinctions and late convergence of gene expression between diapause and quiescence in the Asian tiger mosquito,Aedes albopictus

Poelchau

Reynolds

Elsik

et al. 2013

Journal of Experimental Biology

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SUMMARYDormancy is a crucial adaptation allowing insects to withstand harsh environmental conditions. The pre-programmed developmental arrest of diapause is a form of dormancy that is distinct from quiescence, in which development arrests in immediate response to hardship. Much progress has been made in understanding the environmental and hormonal controls of diapause. However, studies identifying transcriptional changes unique to diapause, rather than quiescence, are lacking, making it difficult to disentangle the transcriptional profiles of diapause from dormancy in general. The Asian tiger mosquito, Aedes albopictus, presents an ideal model for such a study, as diapausing and quiescent eggs can be staged and collected for global gene expression profiling using a newly developed transcriptome. Here, we use RNA-Seq to contrast gene expression during diapause with quiescence to identify transcriptional changes specific to the diapause response. We identify global trends in gene expression that show gradual convergence of diapause gene expression upon gene expression during quiescence. Functionally, early diapause A. albopictus show strong expression differences of genes involved in metabolism, which diminish over time. Of these, only expression of lipid metabolism genes remained distinct in late diapause. We identify several genes putatively related to hormonal control of development that are persistently differentially expressed throughout diapause, suggesting these might be involved in the maintenance of diapause. Our results identify key biological differences between diapausing and quiescent pharate larvae, and suggest candidate pathways for studying metabolism and the hormonal control of development during diapause in other species. Supplementary material available online at

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Hit pause: Developmental arrest in annual killifishes and their close relatives

Martin

Podrabsky

2017

Developmental Dynamics

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Killifishes survive and persist in extreme environments by exploiting both aquatic and terrestrial habitats for egg deposition, and by adjusting the length of development to match availability of water to support larval growth and maturation. Annual killifishes persist in ephemeral bodies of water through the production of drought-tolerant embryos. Survival of the environmental stresses associated with their highly variable and seasonal habitat is supported by their ability to enter into at least two states of metabolic and developmental dormancy, diapause or quiescence. There are three stages of diapause in annual killifishes, one occurring prior to gastrulation, one about midway through development, and one in late pre-hatching embryos. Quiescence may occur at any developmental stage. In addition, delayed hatching is known to occur in close relatives of the annual killifishes, and may be superficially confused with pre-hatching diapause. These types of developmental delay are induced by different cues and serve different purposes in the life history of the species. Thus, it is likely that the molecular mechanisms that induce dormancy and support survival are unique in each case. It is imperative that we properly define these forms of developmental dormancy in our studies in order to put our results into the proper ecological and evolutionary context. Here the unique characteristics of these distinct categories of developmental delay are reviewed. Developmental Dynamics 246:858-866, 2017. © 2017 The Authors Developmental Dynamics published by Wiley Periodicals, Inc. on behalf of American Association of Anatomists.

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Decoupling development and energy flow during embryonic diapause in the cricket,Allonemobius socius

Cited by 40 publications

References 54 publications

Physiological strategies during animal diapause: lessons from brine shrimp and annual killifish

Physiological strategies during animal diapause: lessons from brine shrimp and annual killifish

RNA-Seq reveals early distinctions and late convergence of gene expression between diapause and quiescence in the Asian tiger mosquito,Aedes albopictus

Hit pause: Developmental arrest in annual killifishes and their close relatives

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