Comparisons of developmental processes of air-breathing organs among terrestrial isopods (Crustacea, Oniscidea): implications for their evolutionary origins

TL;DR

This study compares how different air-breathing organs develop in three species of land-dwelling crustaceans to understand their evolutionary origins.

Contribution

The study reveals distinct developmental processes behind two types of air-breathing structures in terrestrial isopods, suggesting different evolutionary mechanisms.

Findings

Uncovered lungs in Nagurus okinawaensis develop from epithelium and cuticle around the hemolymph sinus in post-manca stages.

Dorsal respiratory fields in Alloniscus balssi form from lateral protrusions of ventral epithelium immediately after hatching.

Pleopods in Armadilloniscus cf. ellipticus develop thickened cuticle and hemolymph sinus without specialized morphogenesis.

Abstract

The acquisition of air-breathing organs is one of the key innovations for terrestrialization in animals. Terrestrial isopods, a crustacean lineage, can be interesting models to study the evolution of respiratory organs, as they exhibit varieties of air-breathing structures according to their habitats. However, the evolutionary processes and origins of these structures are unclear, due to the lack of information about their developmental processes. To understand the developmental mechanisms, we compared the developmental processes forming different respiratory structures in three isopod species, i.e., ‘uncovered lungs’ in Nagurus okinawaensis (Trachelipodidae), ‘dorsal respiratory fields’ in Alloniscus balssi (Alloniscidae), and pleopods without respiratory structures in Armadilloniscus cf. ellipticus (Detonidae).

In N. okinawaensis with uncovered lungs, epithelium and cuticle around the proximal hemolymph sinus developed into respiratory structures at post-manca juvenile stages. On the other hand, in Al. balssi with dorsal respiratory fields, the region for the future respiratory structure was already present at manca 1 stage, immediately after hatching, where the lateral protrusion of ventral epithelium occurred, forming the respiratory structure. Furthermore, on pleopods in Ar. cf. ellipticus, only thickened dorsal cuticle and the proximal hemolymph sinus developed during postembryonic development without special morphogenesis.

This study shows that the respiratory structures in terrestrial isopods develop primarily by postembryonic epithelial modifications, but the epithelial positions developing into respiratory structures differ between uncovered lungs and dorsal respiratory fields. This suggests that these two types of respiratory structures do not result from simple differences in the degree of development. Future analysis of molecular developmental mechanisms will help determine whether these are the result of heterotopic changes or have different evolutionary origins. Overall, this study provides fundamental information for evolutionary developmental studies of isopod respiratory organs.

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