Developmental changes in hypoxic exposure and responses to anoxia in Drosophila melanogaster

Viviane Callier, Steven C. Hand, Jacob B. Campbell, Taylor Biddulph, Jon Harrison

Research output: Contribution to journalArticle

24 Citations (Scopus)

Abstract

Holometabolous insects undergo dramatic morphological and physiological changes during ontogeny. In particular, the larvae of many holometabolous insects are specialized to feed in soil, water or dung, inside plant structures, or inside other organisms as parasites where they may commonly experience hypoxia or anoxia. In contrast, holometabolous adults usually are winged and live with access to air. Here, we show that larval Drosophila melanogaster experience severe hypoxia in their normal laboratory environments; third instar larvae feed by tunneling into a medium without usable oxygen. Larvae move strongly in anoxia for many minutes, while adults (like most other adult insects) are quickly paralyzed. Adults survive anoxia nearly an order of magnitude longer than larvae (LT50: 8.3 versus 1 h). Plausibly, the paralysis of adults is a programmed response to reduce ATP need and enhance survival. In support of that hypothesis, larvae produce lactate at 3× greater rates than adults in anoxia. However, when immobile in anoxia, larvae and adults are similarly able to decrease their metabolic rate, to about 3% of normoxic conditions. These data suggest that Drosophila larvae and adults have been differentially selected for behavioral and metabolic responses to anoxia, with larvae exhibiting vigorous escape behavior likely enabling release from viscous anoxic media to predictably normoxic air, while the paralysis behavior of adults maximizes their chances of surviving flooding events of unpredictable duration. Developmental remodeling of behavioral and metabolic strategies to hypoxia/anoxia is a previously unrecognized major attribute of holometabolism.

Original languageEnglish (US)
Pages (from-to)2927-2934
Number of pages8
JournalJournal of Experimental Biology
Volume218
Issue number18
DOIs
StatePublished - Sep 1 2015

Fingerprint

anoxia
Drosophila melanogaster
hypoxia
Larva
larva
larvae
Insects
insect
paralysis
Paralysis
escape behavior
Air
Hypoxia
exposure
Plant Structures
air
insects
normoxia
imagos
ontogeny

Keywords

  • Holometabolism
  • Metabolism
  • Ontogeny
  • PO

ASJC Scopus subject areas

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

Cite this

Developmental changes in hypoxic exposure and responses to anoxia in Drosophila melanogaster. / Callier, Viviane; Hand, Steven C.; Campbell, Jacob B.; Biddulph, Taylor; Harrison, Jon.

In: Journal of Experimental Biology, Vol. 218, No. 18, 01.09.2015, p. 2927-2934.

Research output: Contribution to journalArticle

Callier, Viviane ; Hand, Steven C. ; Campbell, Jacob B. ; Biddulph, Taylor ; Harrison, Jon. / Developmental changes in hypoxic exposure and responses to anoxia in Drosophila melanogaster. In: Journal of Experimental Biology. 2015 ; Vol. 218, No. 18. pp. 2927-2934.
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