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.
Phylogenetic relationships among subgroups of cockroaches and termites are still matters of debate. Their divergence times and major phenotypic transitions during evolution are also not yet settled. We addressed these points by combining the first nuclear phylogenomic study of termites and cockroaches with a thorough approach to divergence time analysis, identification of endosymbionts, and reconstruction of ancestral morphological traits and behaviour. Analyses of the phylogenetic relationships within Blattodea robustly confirm previously uncertain hypotheses such as the sister-group relationship between Blaberoidea and remaining Blattodea, and Lamproblatta being the closest relative to the social and wood-feeding Cryptocercus and termites. Consequently, we propose new names for various clades in Blattodea: Cryptocercus þ termites ¼ Tutricablattae; Lamproblattidae þ Tutricablattae ¼ Kittrickea; and Blattoidea þ Corydioidea ¼ Solumblattodea. Our inferred divergence times
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.
External and internal head structures of adults of Galloisiana yuasai (Grylloblattodea) are described. The results are compared with conditions found in representatives of other lower neopteran lineages, notably in Austrophasma and Karoophasma (both Mantophasmatodea). Sutures and ridges of the head capsule are discussed. A new nomenclature for head muscles is presented for the entire Dicondylia (= Zygentoma + Pterygota). Galloisiana (like its sister taxon Grylloblatta) is mostly characterized by plesiomorphic features, such as the largely unspecialized orthopteroid mouthparts, the multisegmented filiform antennae, the presence of trabeculae tentorii, the absence of muscles associated with the antennal ampullae, the presence of musculus stipitalis transversalis (0mx11) and the presence of musculus tentoriofrontalis anterior (0te2). Autapomorphies of Grylloblattodea are: (i) compound eyes composed of only 60 ommatidia or less; (ii) a lacinia with a proximal tooth; (iii) a rounded submentum; (iv) loss of musculus craniohypopharyngealis (0hy3); and (v) loss of musculus labroepipharyngealis (0lb5). The phylogenetic evaluation of 104 characters of the head yields a branching pattern with Grylloblattodea as a sister group of Mantophasmatodea in clade Xenonomia. Putative synapomorphies of both taxa are: (i) a distinct angle (more than 60 • ) between the submentum and the mentum; (ii) posteriorly oriented labial palpi; (iii) a flat and lobe-like hypopharynx with a suspensorium far ventrad of the anatomical mouth opening; (iv) loss of musculus tentorioparaglossalis (0la6); and (v) a connection between the antennal ampulla and the supraoesophageal ganglion containing nuclei. Xenonomia is placed in a clade with the two dictyopteran terminals. Another monophyletic group is Embioptera + Phasmatodea. Most branches of the single tree obtained in our analysis are weakly supported. The results clearly show that more data and a much broader taxon sampling are required to clarify the phylogenetic interrelationships of the lower neopteran orders. However, our results narrow down the spectrum of possible solutions, and represent a starting point for future phylogenetic analyses, with an extensive concatenated dataset.
Insect wing is a key evolutionary innovation for insect radiation, but its origins and intermediate forms are absent from the fossil record. To understand the ancestral state of the wing, expression of three key regulatory genes in insect wing development, wingless (wg), vestigial (vg), and apterous (ap) was studied in two basal insects, mayfly and bristletail. These basal insects develop dorsal limb branches, tracheal gill and stylus, respectively, that have been considered candidates for wing origin. Here we show that wg and vg are expressed in primordia for tracheal gill and stylus. Those primordia are all located in the lateral body region marked by down-regulation of early segmental wg stripes, but differ in their dorsal-ventral position, indicating their positions drifted within the lateral body region. On the other hand, ap expression was detected in terga of mayfly and bristletail. Notably, the extensive outgrowth of the paranotal lobe of apterygote bristletail developed from the border of ap-expressing tergal margin, and also expressed wg and vg. The data suggest that two regulatory modules involving wg-vg are present in apterygote insects: one associated with lateral body region and induces stick-like dorsal limb branches, the other associated with the boundary of dorsal and lateral body regions and the flat outgrowth of their interface. A combinatorial model is proposed in which dorsal limb branch was incorporated into dorsal-lateral boundary and acquired flat limb morphology through integration of the two wg-vg modules, allowing rapid evolution of the wing.
The embryogenesis of Grylloblattodea, one of the most primitive of the polyneopteran orders, is described using Galloisiana yuasai with special reference to external morphology. The egg membranes are characterized by an endochorion crossed by numerous vertical aeropyles and a fairly thin vitelline membrane, features shared by Mantophasmatodea. The inner layer formation is of the fault type. Serosal elements in the amnioserosal fold differentiate into hydropylar cells, to function in water absorption together with specialized amniotic structures, i.e., an amniotic strand and a thickened amnion. The germ band is of the short germ type. The germ band immerses deep into the yolk after its full elongation along the egg surface, and in this respect blastokinesis closely resembles that of Mantophasmatodea. The embryological features, i.e., those on egg membranes and blastokinesis, may suggest a closer affinity of Grylloblattodea and Mantophasmatodea. Appendages, ectodermal invaginations, and sternal and pleural sclerites are discussed in the light of serial homology, to provide a new basis for elucidating the insect body plan. Appendages are divided into the proximal coxopodite and distal telopodite, the former being divided further into the subcoxa and coxa. Subcoxal and coxal elements are identified in the mandible as well as in the abdominal appendages. The subcoxa is divided into the epimeron and episternum by the pleural suture in thoracic segments. Likewise, in the abdominal segments the subcoxa is divided into two, although the homologs of the epimeron and episternum are not sclerotized, and in the labial segment the subcoxal derivative or the postmentum is divided into the submentum and mentum. Two coxal endites bulge out from the medial side of the gnathal appendages. The mandibular molar and incisor, maxillary lacinia and galea, and labial glossa and paraglossa are serially homologous with each other. In the thoracic segments the original embryonic sternum or "protosternum" is largely replaced by subcoxal elements, and merely remains as a small anterior presternum and a posterior spinasternum. A major part of the venter is represented by the derivatives of the episternum such as an extensive basisternum, katepisternum, and trochantin and the medial element of the epimeron. The pleuron is derived from the episternal elements or the anepisternum and preepisternum, which bears a spiracle in the mesothorax and metathorax, and the lateral element of the epimeron. The homolog of the preepisternum in the prothorax is the cervical sclerite, but with no spiracle developed. A median ventral invagination arises in the thoracic segments as a spina, and the homolog of the spina develops into the eversible sac in the first abdominal segment.
The voltage-gated proton channel 1 (H V 1) is an important component of the cellular proton extrusion machinery and is essential for charge compensation during the respiratory burst of phagocytes. H V 1 has been identified in a wide range of eukaryotes throughout the animal kingdom, with the exception of insects. Therefore, it has been proposed that insects do not possess an H V 1 channel. In the present study, we report the existence of an H V 1-type proton channel in insects. We searched insect transcriptome shotgun assembly (TSA) sequence databases and found putative H V 1 orthologues in various polyneopteran insects. To confirm that these putative H V 1 orthologues were functional channels, we studied the H V 1 channel of Nicoletia phytophila (NpH V 1), an insect of the Zygentoma order, in more detail. NpH V 1 comprises 239 amino acids and is 33% identical to the human voltage-gated proton channel 1. Patch clamp measurements in a heterologous expression system showed proton selectivity, as well as pHand voltage-dependent gating. Interestingly, NpH V 1 shows slightly enhanced pH-dependent gating compared to the human channel. Mutations in the first transmembrane segment at position 66 (Asp66), the presumed selectivity filter, lead to a loss of proton-selective conduction, confirming the importance of this aspartate residue in voltage-gated proton channels.
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