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

Author:

Visser Bertanne12ORCID,Williams Caroline M.23,Hahn Daniel A.2,Short Clancy A.2,López-Martínez Giancarlo24

Affiliation:

1. Evolutionary Ecology and Genetics Group, Biodiversity Research Centre, Earth and Life Institute, Université catholique de Louvain, Croix du Sud 4-5, 1348 Louvain-la-Neuve, Belgium

2. Department of Entomology and Nematology, College of Agriculture and Life Sciences, University of Florida, Gainesville, Florida 32611, USA

3. Department of Integrative Biology, University of California, Berkeley, California 94720. USA

4. Department of Biology, New Mexico State University, Las Cruces, New Mexico 88003, USA

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. While 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 Anastrepha suspensa (Loew)(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 test whether prior anoxia exposures during pupal development can induce a beneficial acclimation response, and we explore 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 to 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.

Funder

Fonds De La Recherche Scientifique - FNRS

National Science Foundation

U.S. Department of Agriculture

National Institute of General Medical Sciences

Publisher

The Company of Biologists

Subject

Insect Science,Molecular Biology,Animal Science and Zoology,Aquatic Science,Physiology,Ecology, Evolution, Behavior and Systematics

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