Evolutionary history of Polyneoptera and its implications for our understanding of early winged insects

Polyneoptera represents one of the major lineages of winged
insects, comprising around 40,000 extant species in 10 traditional
orders, including grasshoppers, roaches, and stoneflies. Many
important aspects of polyneopteran evolution, such as their phylogenetic
relationships, changes in their external appearance, their
habitat preferences, and social behavior, are unresolved and are a
major enigma in entomology. These ambiguities also have direct
consequences for our understanding of the evolution of winged
insects in general; for example, with respect to the ancestral
habitats of adults and juveniles. We addressed these issues with
a large-scale phylogenomic analysis and used the reconstructed
phylogenetic relationships to trace the evolution of 112 characters
associated with the external appearance and the lifestyle of winged
insects. Our inferences suggest that the last common ancestors of
Polyneoptera and of the winged insects were terrestrial throughout
their lives, implying that wings did not evolve in an aquatic
environment. The appearance of the first polyneopteran insect
wasmainly characterized by ancestral traits such as long segmented
abdominal appendages and biting mouthparts held below the head
capsule. This ancestor lived in association with the ground, which
led to various specializations including hardened forewings and
unique tarsal attachment structures. However, within Polyneoptera,
several groups switched separately to a life on plants. In contrast to
a previous hypothesis, we found that social behavior was not part
of the polyneopteran ground plan. In other traits, such as the biting
mouthparts, Polyneoptera shows a high degree of evolutionary
conservatism unique among the major lineages of winged insects.