Abstract
The adaptive significance of discontinuous gas exchange cycles (DGC) in insects is contentious. Based on observations of DGC occurrence in insects of typically large brain size and often socially-complex life history, and spontaneous DGC in decapitated insects, the neural hypothesis for the evolution of DGC was recently proposed. It posits that DGC is a non-adaptive consequence of adaptive down-regulation of brain activity at rest, reverting ventilatory control to pattern-generating circuits in the thoracic ganglia. In line with the predictions of this new hypothesis, we expected a higher likelihood of DGC in the gregarious phase of the desert locust (Schistocerca gregaria, Orthoptera), which is characterized by a larger brain size and increased sensory sensitivity compared with the solitary phase. Furthermore, surgical severing of the neural connections between head and thoracic ganglia was expected to increase DGC prevalence in both phases, and to eliminate phase-dependent variation in gas exchange patterns. Using flow-through respirometry, we measured metabolic rates and gas exchange patterns in locusts at 30°C. In contrast to the predictions of the neural hypothesis, we found no phase-dependent differences in DGC expression. Likewise, surgically severing the descending regulation of thoracic ventilatory control did not increase DGC prevalence in either phase. Moreover, connective-cut solitary locusts abandoned DGC altogether, and employed a typical continuous gas exchange pattern despite maintaining metabolic rate levels of controls. These results are not consistent with the predictions of the neural hypothesis for the evolution of DGC in insects, and instead suggest neural plasticity of ventilatory control.
Highlights
Insects exchange respiratory gases between their tissues and the external environment through a gas-filled tracheal system
In contrast to our prediction for intact individuals, higher discontinuous gas exchange cycles (DGC) prevalence was recorded among the solitary group (Table 1), phase-dependent variation in gas exchange patterns among intact specimens was not statistically significant (x2(df = 2) = 2.647, P = 0.266)
Among the circumstantial evidence lending support to the neural hypothesis, are the typically larger brain sizes in species belonging to the five insect orders in which DGC has been observed
Summary
Insects exchange respiratory gases between their tissues and the external environment through a gas-filled tracheal system. The tracheal system opens to the external environment through paired spiracles, located laterally on the thoracic and abdominal segments of the insect body ]1[. Most insects control spiracular opening through closer/opener muscles, with a resulting variety of gas exchange patterns. These have been categorized as: (i) continuous gas exchange, where spiracles remain constantly opened, or flutter at high-frequency; (ii) cyclic gas exchange, where spiracles open and close intermittently; and (iii) discontinuous gas exchange cycles (DGC), characterized by prolonged closure of the spiracles, during which gas exchange is generally undetectable ]2[. The adaptive value of DGC, contributing to its evolutionary origin and maintenance in insects and other tracheated terrestrial arthropods, is contentious, and has long been the subject of scientific controversy (reviewed by [2], [5,6,7])
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