Handling and Use of Oxygen by Pancrustaceans: Conserved Patterns and the Evolution of Respiratory Structures.

The handling and use of oxygen are central to physiological function of all pancrustaceans. Throughout the Pancrustacea, ventilation is controlled by a central oxygen-sensitive pattern generator. The ancestral condition was likely to achieve ventilation of the gills via leg-associated or mouth-associated muscles, but in insects and some air-breathing crustaceans, new muscles were recruited for this purpose, including intersegmental muscles likely used previously for posture and locomotion. Many aspects of the sensing of oxygen and the occurrence of responses to hypoxia (increased ventilation, depressed growth and metabolic rate, developmental changes that enhance the delivery of oxygen) appear common across most pancrustaceans, but there is tremendous variation across species. Some of this can be explained by habitat (e.g., ventilation of the internal medium occurs in terrestrial species and of the external medium in aquatic species; rearing under hypoxia induces tracheal proliferation in terrestrial insects and hemocyanin production in aquatic crustaceans); some plausibly by evolutionary origin of some responses to hypoxia within the Pancrustacea (the most basal arthropods may lack a ventilatory response to hypoxia); and some by the availability of environmental oxygen (animals adapted to survive hypoxia turn on the response to hypoxia at a lower PO2). On average, crustaceans and insects have similar tolerances to prolonged anoxia, but species or life stages from habitats with a danger of being trapped in hypoxia can tolerate longer durations of anoxia. Lactate is the primary anaerobic end-product in crustaceans but some insects have evolved a more diverse array of anaerobic end-products, including ethanol, alanine, succinate, and acetate. Most clades of Pancrustacea are small and lack obvious respiratory structures. Gilled stem-pancrustaceans likely evolved in the Cambrian, and gills persist in large Ostracoda, Malacostraca, and Branchiopoda. Based on currently accepted phylogenies, invaginations of cuticle to form lungs or tracheae occurred independently multiple times across the Arthropoda and Pancrustacea in association with the evolution of terrestriality. However, the timing and number of such events in the evolution of tracheal systems remain controversial. Despite molecular phylogenies that place the origin of the hexapods before the appearance of land plants in the Ordovician, terrestrial fossils of Collembola, Archaeognatha, and Zygentoma in the Silurian and Devonian, and the lack of fossil evidence for older aquatic hexapods, suggest that the tracheated hexapods likely evolved from Remipedia-like ancestors on land.