Is flight architecture determined by physical constraints or by natural selection?: the case of the midge Chironomus plumosus

Males of the midge Chironomus plumosus fly solely to mate. They maintain station for long periods in moving air. Females patrol in search of males and, after receiving a spermatophore, fly to oviposition sites. The requirements of flight in males and females are therefore fundamentally different. Females are larger than males, on average, so these differences could stem from scaling rules governing the geometry of space. The same explanation might apply to flight differences within the sexes and even to peculiarities of flight architecture in C. plumosus compared to other flying animals. In other words, might flight design be accounted for entirely by mechanical constraints without recourse to natural selection? To test this hypothesis, the power output of C. plumosu was measured as size‐specific muscle mass. Contrary to expectation, little evidence was found of scaling effects in this measure of power. Despite its being among the smallest of animals to fly, C. plumosus turns out to have the largest mass of flight muscle, relative to body size, yet found among animals. Differences both between C. plumosus and other species and within C. plumosus are, in general, more readily accounted for by the requirements of the mating system within the viscous universe encountered by small flying animals. We conclude that it is natural selection rather than mechanical constraint that is the primary influence determining the architecture of flight in this small animal.