Insects have a unique respiratory system; their tissues are in direct contact with the atmosphere through a branched network of tubules, and airflow into and out of the tubules is controlled by spiracles, valve-like structures at the body surface. Intriguingly, insect spiracles open and close in a cyclical pattern called the discontinuous gas exchange cycle. In the first phase of the cycle, which can last for long periods, the respiratory system is fully closed and oxygen partial pressure (PO2)within the tubules drops as tissues consume oxygen, while CO2partial pressure (PCO2) increases as a result of respiration. When the spiracles start fluttering, limited gas exchange occurs. In the final phase, the spiracles are fully opened and the PO2 and PCO2within the tubules reach atmospheric levels.
Two theories dominate the ongoing debate over the evolution of the discontinuous gas exchange cycle. The first claims that this respiration pattern limits water loss, while the second argues that it initially evolved in underground environments with low PO2 and high PCO2, where the cycle augments the PO2 and PCO2exchange gradient. However, these theories cannot be reconciled with experimental results.
Now, Stefan Hetz and Timothy Bradley propose a new theory to explain the evolution of the discontinuous gas exchange cycle. They claim that this cycle evolved to limit the generation of reactive oxygen species, toxic compounds that cause oxidative damage to tissues. They suggest that the intentional exclusion of O2 drives the cyclical nature of insect respiration.
One prediction arising from Hetz and Bradley's suggestion is that the open phase of the cycle should lead to sufficiently high internal PO2 to cause oxidative damage. To test this,the team recorded PO2 inside moth pupae's tubules during the open phase, and found that the insect's tissues are exposed to PO2 around 19 kPa. Given that vertebrate tissues are normally exposed to PO2 between 0.5–5 kPa, this is an extremely high oxygen concentration. Clearly,tissues exposed to these high oxygen levels for prolonged periods would suffer considerable oxidative damage, lending support to Hetz and Bradley's hypothesis.
To test a second prediction of their hypothesis, that atmospheric oxygen levels regulate the cyclical respiration pattern, Hetz and Bradley exposed moth pupae to various oxygen levels and examined the regulation of respiration. They observed that the insects' spiracles opened much more frequently at low O2 levels than at normal O2 levels,while they almost never opened when the team exposed the insects to high O2 levels. This indicates that environmental oxygen concentration does regulate insect respiratory behaviour.
Finally, the pair needed to show that the discontinuous gas exchange cycle helps insects keep their tubule PO2 levels high enough for mitochondrial respiration, but low enough to limit oxidative damage. Hetz and Bradley showed that moth pupae keep their spiracles closed for long periods and then open them briefly to permit O2 entry,which serves to keep the O2 concentration within their tubules close to 4 kPa. So these insects do manage to regulate internal PO2 at a level that promotes efficient mitochondrial metabolism without generating excessive oxidative damage.
The authors reflect on the reason for the evolution of a respiratory pattern that imposes oxidative stress in insects. The key observation is that the discontinuous gas exchange cycle is present only when insects rest. The team concludes, `the respiratory pattern that we observe during low demand is the insect's attempt to use a high capacity system during periods of metabolic idling.'