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Integrated phylogenomic and fossil evidence of stick and leaf insects (Phasmatodea) reveal a Permian-Triassic co-origination with insectivores.

ABSTRACT: Stick and leaf insects (Phasmatodea) are a distinctive insect order whose members are characterized by mimicking various plant tissues such as twigs, foliage and bark. Unfortunately, the phylogenetic relationships among phasmatodean subfamilies and the timescale of their evolution remain uncertain. Recent molecular clock analyses have suggested a Cretaceous-Palaeogene origin of crown Phasmatodea and a subsequent Cenozoic radiation, contrasting with fossil evidence. Here, we analysed transcriptomic data from a broad diversity of phasmatodeans and, combined with the assembly of a new suite of fossil calibrations, we elucidate the evolutionary history of stick and leaf insects. Our results differ from recent studies in the position of the leaf insects (Phylliinae), which are recovered as sister to a clade comprising Clitumninae, Lancerocercata, Lonchodinae, Necrosciinae and Xenophasmina. We recover a Permian to Triassic origin of crown Phasmatodea coinciding with the radiation of early insectivorous parareptiles, amphibians and synapsids. Aschiphasmatinae and Neophasmatodea diverged in the Jurassic-Early Cretaceous. A second spur in origination occurred in the Late Cretaceous, coinciding with the Cretaceous Terrestrial Revolution, and was probably driven by visual predators such as stem birds (Enantiornithes) and the radiation of angiosperms.

SUBMITTER: Tihelka E

PROVIDER: S-EPMC7735357 | biostudies-literature | 2020 Nov

REPOSITORIES: biostudies-literature

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Integrated phylogenomic and fossil evidence of stick and leaf insects (Phasmatodea) reveal a Permian-Triassic co-origination with insectivores.

Tihelka Erik E Cai Chenyang C Giacomelli Mattia M Pisani Davide D Donoghue Philip C J PCJ

Royal Society open science 20201111 11

Stick and leaf insects (Phasmatodea) are a distinctive insect order whose members are characterized by mimicking various plant tissues such as twigs, foliage and bark. Unfortunately, the phylogenetic relationships among phasmatodean subfamilies and the timescale of their evolution remain uncertain. Recent molecular clock analyses have suggested a Cretaceous-Palaeogene origin of crown Phasmatodea and a subsequent Cenozoic radiation, contrasting with fossil evidence. Here, we analysed transcriptom ...[more]

PMID: 33391817

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Project description:BackgroundPhasmatodea are well known for their ability to disguise themselves by mimicking twigs, leaves, or bark, and are therefore commonly referred to as stick and leaf insects. In addition to this and other defensive strategies, many phasmatodean species use paired prothoracic repellent glands to release defensive chemicals when disturbed by predators or parasites. These glands are considered as an autapomorphic trait of the Phasmatodea. However, detailed knowledge of the gland anatomy and chemical compounds is scarce and only a few species were studied until now. We investigated the repellent glands for a global sampling of stick and leaf insects that represents all major phasmatodean lineages morphologically via µCT scans and analyzed the anatomical traits in a phylogenetic context.ResultsAll twelve investigated species possess prothoracic repellent glands that we classify into four distinct gland types. 1: lobe-like glands, 2: sac-like glands without ejaculatory duct, 3: sac-like glands with ejaculatory duct and 4: tube-like glands. Lobe-like glands are exclusively present in Timema, sac-like glands without ejaculatory duct are only found in Orthomeria, whereas the other two types are distributed across all other taxa (= Neophasmatodea). The relative size differences of these glands vary significantly between species, with some glands not exceeding in length the anterior quarter of the prothorax, and other glands extending to the end of the metathorax.ConclusionsWe could not detect any strong correlation between aposematic or cryptic coloration of the examined phasmatodeans and gland type or size. We hypothesize that a comparatively small gland was present in the last common ancestor of Phasmatodea and Euphasmatodea, and that the gland volume increased independently in subordinate lineages of the Occidophasmata and Oriophasmata. Alternatively, the stem species of Neophasmatodea already developed large glands that were reduced in size several times independently. In any case, our results indicate a convergent evolution of the gland types, which was probably closely linked to properties of the chemical components and different predator selection pressures. Our study is the first showing the great anatomical variability of repellent glands in stick and leaf insects.

Project description:Simple Summary Herbivorous insects and plants greatly affected each other’s evolution due to their close interactions. This resulted in the development of a variety of adaptations on both sides. Through the need for protection against herbivorous insects, surfaces with lower attachment ability evolved in many plants. As a response, the attachment systems of insects have developed numerous specializations. Stick insects (Phasmatodea) have an attachment system, consisting of paired claws, arolium (attachment pad between the claws) and euplantulae (paired attachment pads on the tarsomeres), which is well adapted to different natural surfaces. We used measurements of pull-off and traction force in two species (Medauroidea extradentata and Sungaya inexpectata) representing the most common microstructures used for attachment within stick insects (nubby and smooth) to quantify the attachment ability of Phasmatodea on natural surfaces. Plant leaves with different surface properties (smooth, trichome-covered, hydrophilic and covered with crystalline waxes) were selected as substrates. Wax-crystal-covered fine-roughness substrates revealed the lowest, whereas strongly structured substrates showed the highest attachment performance among the stick insects studied. Removing the claws of the insects resulted in lower attachment ability on structured substrates. Furthermore, claw removal revealed that the attachment performance of the pads is less reduced by contaminating wax crystals in the species with nubby attachment structures. Long-lasting effects of the leaves on the attachment ability were briefly investigated, but not confirmed. Abstract Herbivorous insects and plants exemplify a longstanding antagonistic coevolution, resulting in the development of a variety of adaptations on both sides. Some plant surfaces evolved features that negatively influence the performance of the attachment systems of insects, which adapted accordingly as a response. Stick insects (Phasmatodea) have a well-adapted attachment system with paired claws, pretarsal arolium and tarsal euplantulae. We measured the attachment ability of Medauroidea extradentata with smooth surface on the euplantulae and Sungaya inexpectata with nubby microstructures of the euplantulae on different plant substrates, and their pull-off and traction forces were determined. These species represent the two most common euplantulae microstructures, which are also the main difference between their respective attachment systems. The measurements were performed on selected plant leaves with different properties (smooth, trichome-covered, hydrophilic and covered with crystalline waxes) representing different types among the high diversity of plant surfaces. Wax-crystal-covered substrates with fine roughness revealed the lowest, whereas strongly structured substrates showed the highest attachment ability of the Phasmatodea species studied. Removal of the claws caused lower attachment due to loss of mechanical interlocking. Interestingly, the two species showed significant differences without claws on wax-crystal-covered leaves, where the individuals with nubby euplantulae revealed stronger attachment. Long-lasting effects of the leaves on the attachment ability were briefly investigated, but not confirmed.

Dataset Information

Integrated phylogenomic and fossil evidence of stick and leaf insects (Phasmatodea) reveal a Permian-Triassic co-origination with insectivores.

Publications

Integrated phylogenomic and fossil evidence of stick and leaf insects (Phasmatodea) reveal a Permian-Triassic co-origination with insectivores.

Similar Datasets

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