The Evolution of Flightlessness in Insects

Many pterygote (winged) insects have secondarily become flightless; why has this occurred? In this paper I test for an association between the frequency of flightlessness and (1) environmental heterogeneity, (2) geographic variables, (3) gender, (4) alternate modes of migration, and (5) taxonomic variation. Various authors have predicted that decreased environmental heterogeneity will favor the evolution of flightlessness. This hypothesis is consistent with a number of studies on the variation of wing dimorphism and flightlessness and with data analyzed in the present paper on the relationship between habitat type and wing morph in the North American Orthoptera. The incidence of flightlessness is also exceptionally high in woodlands, deserts, on the ocean surface, in specific habitats on the seashore (dunes and rock crevices but not the foreshore), in aquatic habitats, in the winter months, in hymenopteran and termite nests, and among ectoparasites of endotherms and parasites of arthropods. It is low in habitats bordering rivers, streams, ponds, etc. and in arboreal habitats. Some of these habitats can be classified as persistent, but others cannot be so designated or are too vaguely defined. The incidence of flightlessness increases with altitude and latitude but, contrary to "conventional" wisdom, it is not exceptionally high on oceanic islands compared to mainland areas. Several authors have hypothesized that the clinal variation in flightlessness is a consequence of clinal variation in habitat persistence. Though the available data are consistent with this hypothesis, other factors such as impairment of flight by low temperatures cannot be rejected, though considered unlikely. Flightlessness is more frequent than expected by chance among parthenogenetic species and more frequent among females than males. Furthermore, there is a significant negative association between female mobility and flightlessness in males. I suggest that loss of flight is favored in females because it permits greater allocation of resources to egg production, but that flight is retained in males because it increases the probability of finding a mate. In some species alternate modes of migration, viz phoresy and ballooning, have evolved. Phoretic transport (i.e., via other animal species) may be important in those species in which it occurs, but it appears to have evolved relatively rarely. Among the Insecta ballooning occurs only in the larvae of Lepidoptera. Aptery (winglessness) is unusually frequent among Lepidoptera that eclose in the fall and winter months and live in woodlands and forests. I hypothesize that larval migration by ballooning, the large—scale spatiotemporal stability of woodlands, and the small—scale unpredictability of spring bud burst are primary factors favoring the evolution of flightlessness in these Lepidoptera. The mode of metamorphosis is correlated with the frequency of flightlessness; hemimetabolous and holometabolous insects are rarely flightless, while it is common among paurometabolous insects. Two factors that may favor such an association are differences in relative mobility of the larvae and niche shifts between the adult and larval stage. In the holometabolous insects taxonomic families with at least one flightless species have more species than those with only winged species. A possible explanation for this is that the occurrence of the appropriate ecological conditions favoring flightlessness in holometabolous insects and the requisite mutations are both very rare events.