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

Abstract

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 was mainly 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.

The evolution of Zoraptera

“…Recently, Wipfler et al . () reconstructed the morphology of the common ancestor of Polyneoptera and subsequent evolutionary developments, based on a robust phylogenetic hypothesis congruent with Misof et al . ().…”

“…The group is mainly distributed in subtropical and tropical regions (Grimaldi & Engel, ; Beutel et al ., ; Mashimo et al ., ; Choe, ). Its phylogenetic position has been controversial (reviewed in Mashimo et al ., ; Kjer et al ., ; Beutel et al ., ), with consensus apparently reached recently with Zoraptera being placed in a monophyletic Polyneoptera based on different sources of evidence (Yoshizawa, ; Misof et al ., ; Wipfler & Pass, ; Mashimo et al ., , ; Matsumura et al ., ; Wipfler et al ., ). Recently, Wipfler et al .…”

“…They recovered Zoraptera as the sister group of Dermaptera, and both orders were placed as sister to the rest of the polyneopteran orders. They also postulated that the last common ancestor of Polyneoptera was ‘a ground‐dwelling insect with a largely unmodified body relative to the last common ancestor of winged insects’ (Wipfler et al ., ). Considering the winged morphs of Zoraptera (e.g.…”

“…They lack any conspicuous features with the exceptions of a very distinct dimorphism (apterous and alate morphs) and extremely varying genitalia (Mashimo et al ., ; Choe, ). Considering the assumed reconstructed common ancestor of Polyneoptera (Wipfler et al ., ), Zoraptera have apparently acquired a lifestyle characterized by cryptic habitats, gregarious behaviour and miniaturization. However, their evolutionary origin and morphological transformations over time are still largely obscure.…”

Multifunctional cellulase enzymes are ancestral in Polyneoptera

“…The present study aims to understand the evolutionary history of the special abilities to digest plants in Phasmatodea. Recent transcriptomic studies further supported the idea that the webspinners (Embioptera) form the sister group of Phasmatodea (Misof et al ., ; Wipfler et al ., ). They are a small group of winged Polyneoptera with fewer than 400 out of an estimated 2000 species described (Szumik et al ., ).…”