Yuta Mashimo

Insects are the most speciose group of animals, but the phylogenetic relationships of many major lineages remain unresolved. We inferred the phylogeny of insects from 1478 protein-coding genes. Phylogenomic analyses of nucleotide and amino acid sequences, with site-specific nucleotide or domain-specific amino acid substitution models, produced statistically robust and congruent results resolving previously controversial phylogenetic relations hips. We dated the origin of insects to the Early Ordovician [~479 million years ago (Ma)], of insect flight to the Early Devonian (~406 Ma), of major extant lineages to the Mississippian (~345 Ma), and the major diversification of holometabolous insects to the Early Cretaceous. Our phylogenomic study provides a comprehensive reliable scaffold for future comparative analyses of evolutionary innovations among 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 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.

Zoraptera are a cryptic and enigmatic group of insects. The species diversity is lower than in almost all other groups of Hexapoda, but may be distinctly higher than presently known. Several new species were described from different regions recently. The systematic placement was discussed controversially since the group was discovered 100 years ago. Affinities with Isoptera and Psocoptera were discussed in earlier studies. A sister group relationship with Acercaria (Psocodea, Thysanoptera, Hemiptera) was proposed by W. Hennig, for the first time based on a strictly phylogenetic argumentation. More recent studies consistently suggest a placement among the “lower neopteran orders” (Polyneoptera). Close affinities to Dictyoptera were proposed and alternatively a sister group relationship with Embioptera or with Embioptera + Phasmatodea (Eukinolabia), respectively. The precise placement is still controversial and the intraordinal relationships are largely unclear. Recent transcriptome analyses tentatively suggest a clade Zoraptera + Dermaptera as sister group of all other polyneopteran orders. The oldest fossils are from Cretaceous amber. An extinct genus from this era may be the sister group of all the remaining zorapterans. The knowledge of the morphology, development and features related to the reproductive system greatly increased in recent years. The general body morphology is very uniform, whereas the genitalia differ strongly between species. This is likely due to different kinds of selection, i.e. sexual selection in the case of the genital organs. The mating pattern also differs profoundly within the order. A unique external sperm transfer occurs in Zorotypus impolitus . A species-level phylogeny and more investigations of the reproductive system should have high priority.