Hormetic benefits of prior anoxia exposure in buffering anoxia stress in a soil-pupating insect

Abstract

Oxygen is essential for most animals, and exposure to a complete lack of oxygen, i.e. anoxia, can result in irreparable damage to cells that can extend up to the organismal level to negatively affect performance. Although it is known that brief anoxia exposure may confer cross-tolerance to other stressors, few data exist on the biochemical and organismal consequences of repeated intermittent bouts of anoxia exposure. In nature, the Caribbean fruit fly, (Diptera: Tephritidae), is frequently exposed to heavy tropical rainfall while pupating in the soil, equating to multiple exposures to hypoxia or anoxia during development. Here, we tested whether prior anoxia exposures during pupal development can induce a beneficial acclimation response, and we explored the consequences of prior exposure for both whole-organism performance and correlated biochemical metrics. Pharate adults (the last developmental stage in the pupal case) were most sensitive to anoxia exposure, showing decreased survival and fertility compared with controls. These negative impacts were ameliorated by exposure to anoxia in earlier pupal developmental stages, indicating a hormetic effect of prior anoxia exposure. Anoxia exposure early in pupal development reduced the oxygen debt repaid after anoxia exposure relative to pharate adults experiencing anoxia for the first time. Lipid levels were highest in all pupal stages when exposed to prior anoxia. Prior anoxia thus benefits organismal performance and relocates resources towards lipid storage throughout pupal-adult development.

Repeat exposure to hypercapnic seawater modifies growth and oxidative status in a tolerant burrowing clam

“…can elicit experience-mediated resilience for a variety of taxa (i.e. fruit fly, coral, fish, zebra finch, mice) increasing CSR, fitness and compensatory/anticipatory responses under subsequent stress exposures (Brown et al, 2002;Costantini et al, 2012;Jonsson and Jonsson, 2014;Visser et al, 2018;Zhang et al, 2018). Further, early-life development presents a sensitive stage to elicit adaptive phenotypic adjustments (Fawcett and Frankenhuis, 2015), prompting investigation of environmental stress acclimation under a rapidly changing environment.…”

Metabolic Recovery and Compensatory Shell Growth of Juvenile Pacific Geoduck Panopea Generosa Following Short-Term Exposure to Acidified Seawater

“…This hormetic-like response (Calabrese et al , 2007; Costantini, 2014) demonstrates a benefit of early stress-priming for later performance and the adaptive plasticity of P. generosa to elevated p CO 2 . Use of hormesis to conceptualize carry over effects of mild stress exposure is largely confined to model insects, plants, and microorganisms (Lee et al , 1987; Calabrese and Blain, 2009; López-Martínez and Hahn, 2012; Visser et al , 2018). For example, Visser et al (Visser et al , 2018) found the Caribbean fruit fly, Anastrepha suspensa , exposed to oxidative stress early in life enhanced survivorship and investment in fertility and lipid synthesis under subsequent stress during adulthood.…”

“…Use of hormesis to conceptualize carry over effects of mild stress exposure is largely confined to model insects, plants, and microorganisms (Lee et al , 1987; Calabrese and Blain, 2009; López-Martínez and Hahn, 2012; Visser et al , 2018). For example, Visser et al (Visser et al , 2018) found the Caribbean fruit fly, Anastrepha suspensa , exposed to oxidative stress early in life enhanced survivorship and investment in fertility and lipid synthesis under subsequent stress during adulthood. Further mechanistic molecular and biochemical assessments under different stress intensities (i.e.…”

“…Hormesis is a biphasic low-dose-stimulatory response, as identified in toxicological studies (Calabrese, 2008), and suggests beneficial carryover effects of moderate stress exposure (Calabrese et al , 2007; Costantini et al , 2010; Costantini, 2014; Putnam et al , 2018). Conditioning-hormesis can explain patterns of inter- and transgenerational plasticity for organisms under environmental change (Calabrese and Mattson, 2011; Costantini et al , 2012; López-Martínez and Hahn, 2012; Putnam et al , 2018; Visser et al , 2018), but is understudied for stress resilience in bivalves likely due to generally negative physiological implications of acidification (Gazeau et al , 2013). In one example of early-life stage conditioning in bivalves, Putnam et al (2017) found P. generosa exhibit compensatory shell growth after an acute exposure under elevated p CO 2 .…”

Early-life hypoxia alters adult physiology and reduces stress resistance and lifespan in Drosophila

“…For example, starvation stress in larval honeybees leads to subsequent starvation tolerance as adults (Wang et al, 2016b;Wang et al, 2016a). In a similar manner, anoxia exposure during the development of the Caribbean fruit fly confers later anoxia resistance in adults (Visser et al, 2018). Early life mild heat stress in the zebra finch has also been shown to lower oxidative damage induced by heat stress in adult life (Costantini et al, 2012).…”