How to be a Giant: Hypermetric Scaling of the Leg in Cockroaches and Scarab Beetles Suggests Oxygen Transport to the Legs Limits Maximal Insect Size

Abstract

Understanding the causes and consequences of the evolution of large or small body size remains one of the important challenges of evolutionary biology. Insects have an unusual respiratory system, transporting oxygen in the gas phase via air‐filled tracheae. The possession of this unique system has been hypothesized to limit insect size, but how the morphology of the tracheal system changes as insects vary in size is still poorly known. Based on comparisons with vertebrates, we expect either geometric isometry in scaling (as found in lungs) or hypometric scaling (as found in vertebrate capillaries), with the latter matching the hypometric scaling of metabolic rate found for most animals. We tested these expectations by measuring the 3D morphology of tracheal systems of ten species each of cockroaches and scarab beetles. In both groups, body mass varied by more than an order of magnitude across species, which included some of the largest extant species of insect. Cockroaches were imaged at Argonne National Laboratory using synchrotron x‐ray microcomputed tomography (SR‐μCT), and scarab beetles were imaged at Virginia Tech using tabletop μCT. We measured the fraction of body volume occupied by the tracheal system for the major body compartments. In general, the tracheal system scaled isometrically in the head, thorax, and abdomen. However, within the legs, tracheal volume scaled strongly hypermetrically, resulting from an increase in number (in roaches) and size (in scarabs) of tracheae and/or air sacs. These data strongly suggest that evolution of larger species of insects requires increased relative investment in the tracheal system of the legs to overcome the challenges of long‐distance transport to muscles and nerves located in these long, blind‐ended structures, limiting the maximal size of insects. Support or Funding Information Supported by NSF IOS 1122157 and IOS 1558052.