Functional differentiation of appendages is one of the factors contributing to the success of arthropods. During evolution, many arthropod lineages have colonized on land and independently acquired air-breathing organs, such as book lungs in chelicerates and tracheae in myriapods and insects. The location of the organs and some gene expression patterns suggest that these respiratory organs are derived from the appendages of ancestors. However, the processes or mechanisms of the evolution remain unclear because the morphologies of these respiratory organs have been largely modified from the normal appendages.
Among arthropods, terrestrial isopods (Malacostraca, Isopoda, Oniscidea) are known to have specialized structures for air breathing in their abdominal appendages (pleopods), called pleopodal lungs or pseudotrachea. Depending on habitats, the structure of respiratory surface area on the pleopods varies. These can be categorized into three types, i.e., covered lungs, uncovered lungs, and dorsal respiratory fields. These diverse isopod lungs allow us to study the evolutionary processes of respiratory organs associated with terrestrialization.
To date, comparative morphological studies have been the primary approach to elucidating lung evolution, while less is known about the detailed developmental processes of lungs. In this study, we compared the developmental process of respiratory organs among terrestrial isopods to identify novel developmental mechanisms that contribute to the acquisition of lungs. We performed morphological and histological observations on three species with three different types of respiratory organs (covered lungs: Porcellio scaber, uncovered lungs: Nagurus okinawaensis, and dorsal respiratory fields: Alloniscus balssi) and one species without lungs (Armadilloniscus ellipticus).
The results revealed that in P. scaber, the epithelial tissue near the base of the pleopods invaginated during the postembryonic manca stages and developed the lung structure. In N. okinawaensis, the respiratory region appeared after the manca stages through the formation of wrinkled epithelium. In addition, in A. balssi, the respiratory region appeared near the base of the pleopods immediately after hatching and gradually expanded. In contrast, A. ellipticus did not develop any specialized structure in their pleopods. The lungs of these isopod species generally developed by modification of the region near the base of the pleopods. On the other hand, the formation timings the epithelial transition of respiratory regions were different among species. These results suggest that the specific region of pleopods that becomes the lungs in derived lineage was already present in the ancestral pleopods, and lung-bearing lineage acquired the novel developmental mechanisms that transformed the region into a complex lung structure.