ABSTRACT
The end-Permian mass extinction (EPME) led to a severe terrestrial ecosystem collapse. However, the ecological response of insects-the most diverse group of organisms on Earth-to the EPME remains poorly understood. Here, we analyse beetle evolutionary history based on taxonomic diversity, morphological disparity, phylogeny, and ecological shifts from the Early Permian to Middle Triassic, using a comprehensive new dataset. Permian beetles were dominated by xylophagous stem groups with high diversity and disparity, which probably played an underappreciated role in the Permian carbon cycle. Our suite of analyses shows that Permian xylophagous beetles suffered a severe extinction during the EPME largely due to the collapse of forest ecosystems, resulting in an Early Triassic gap of xylophagous beetles. New xylophagous beetles appeared widely in the early Middle Triassic, which is consistent with the restoration of forest ecosystems. Our results highlight the ecological significance of insects in deep-time terrestrial ecosystems.
Subject(s)
Biological Evolution , Coleoptera/classification , Extinction, Biological , Animals , Biodiversity , Coleoptera/anatomy & histology , Forests , Herbivory , Phylogeny , Wings, Animal/anatomy & histologyABSTRACT
The order Coleoptera (beetles) is arguably the most speciose group of animals, but the evolutionary history of beetles, including the impacts of plant feeding (herbivory) on beetle diversification, remain poorly understood. We inferred the phylogeny of beetles using 4,818 genes for 146 species, estimated timing and rates of beetle diversification using 89 genes for 521 species representing all major lineages and traced the evolution of beetle genes enabling symbiont-independent digestion of lignocellulose using 154 genomes or transcriptomes. Phylogenomic analyses of these uniquely comprehensive datasets resolved previously controversial beetle relationships, dated the origin of Coleoptera to the Carboniferous, and supported the codiversification of beetles and angiosperms. Moreover, plant cell wall-degrading enzymes (PCWDEs) obtained from bacteria and fungi via horizontal gene transfers may have been key to the Mesozoic diversification of herbivorous beetles-remarkably, both major independent origins of specialized herbivory in beetles coincide with the first appearances of an arsenal of PCWDEs encoded in their genomes. Furthermore, corresponding (Jurassic) diversification rate increases suggest that these novel genes triggered adaptive radiations that resulted in nearly half of all living beetle species. We propose that PCWDEs enabled efficient digestion of plant tissues, including lignocellulose in cell walls, facilitating the evolution of uniquely specialized plant-feeding habits, such as leaf mining and stem and wood boring. Beetle diversity thus appears to have resulted from multiple factors, including low extinction rates over a long evolutionary history, codiversification with angiosperms, and adaptive radiations of specialized herbivorous beetles following convergent horizontal transfers of microbial genes encoding PCWDEs.
Subject(s)
Biodiversity , Biological Evolution , Coleoptera/genetics , Gene Transfer, Horizontal , Genome, Insect , Animals , Bacteria/enzymology , Bacteria/genetics , Bacterial Proteins/genetics , Bacterial Proteins/metabolism , Cell Wall/chemistry , Cell Wall/metabolism , Cellulases/genetics , Cellulases/metabolism , Coleoptera/enzymology , Coleoptera/microbiology , Fungal Proteins/genetics , Fungal Proteins/metabolism , Fungi/enzymology , Fungi/genetics , Herbivory/genetics , Insect Proteins/genetics , Insect Proteins/metabolism , Lignin/chemistry , Lignin/metabolism , Phylogeny , Plants/chemistry , Polysaccharide-Lyases/genetics , Polysaccharide-Lyases/metabolism , Polysaccharides/chemistry , Polysaccharides/metabolismABSTRACT
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.
Subject(s)
Biological Evolution , Insecta/physiology , Neoptera/physiology , Wings, Animal/physiology , Animals , Insecta/genetics , Neoptera/genetics , PhylogenyABSTRACT
BACKGROUND: Gyrinidae are a charismatic group of highly specialized beetles, adapted for a unique lifestyle of swimming on the water surface. They prey on drowning insects and other small arthropods caught in the surface film. Studies based on morphological and molecular data suggest that gyrinids were the first branch splitting off in Adephaga, the second largest suborder of beetles. Despite its basal position within this lineage and a very peculiar morphology, earliest Gyrinidae were recorded not earlier than from the Upper Triassic. RESULTS: Tunguskagyrus. with the single species Tunguskagyrus planus is described from Late Permian deposits of the Anakit area in Middle Siberia. The genus is assigned to the stemgroup of Gyrinidae, thus shifting back the minimum age of this taxon considerably: Tunguskagyrus demonstrates 250 million years of evolutionary stability for a very specialized lifestyle, with a number of key apomorphies characteristic for these epineuston predators and scavengers, but also with some preserved ancestral features not found in extant members of the family. It also implies that major splitting events in this suborder and in crown group Coleoptera had already occurred in the Permian. Gyrinidae and especially aquatic groups of Dytiscoidea flourished in the Mesozoic (for example Coptoclavidae and Dytiscidae) and most survive until the present day, despite the dramatic "Great Dying" - Permian-Triassic mass extinction, which took place shortly (in geological terms) after the time when Tunguskagyrus lived. CONCLUSIONS: Tunguskagyrus confirms a Permian origin of Adephaga, which was recently suggested by phylogenetic "tip-dating" analysis including both fossil and Recent gyrinids. This also confirms that main splitting events leading to the "modern" lineages of beetles took place before the Permian-Triassic mass extinction. Tunguskagyrus shows that Gyrinidae became adapted to swimming on the water surface long before Mesozoic invasions of the aquatic environment took place (Dytiscoidea). The Permian origin of Gyrinidae is consistent with a placement of this highly derived family as the sister group of all remaining adephagan groups, as suggested based on morphological features of larvae and adults and recent analyses of molecular data.
Subject(s)
Biological Evolution , Coleoptera/physiology , Extinction, Biological , Fossils , Animals , Coleoptera/anatomy & histology , Paleontology , Phylogeny , Siberia , Time FactorsABSTRACT
Insects use different parts of their body to cling to mating partners, to catch prey, or to defend themselves, in most cases the mouthparts or the legs. However, in 400 million years of evolution [1, 2], specialized devices were independently acquired in several groups to adopt these tasks, as for instance modified legs in mantids, assassin bugs or stick insects [3-5], or clasping antennae of the globular springtails [6]. So far, no known species used the neck region between the head and thorax in one of these functional contexts. Here we describe females of Caputoraptor elegans, a very unusual, presumably predacious insect discovered in approximately 100-million-year-old [7] Burmese amber. Based on several morphological features, we conclude that this species lived in the foliage of trees or bushes. A unique feature of the new taxon is a scissor-like mechanism formed by wing-like extensions on the posterior head and corresponding serrated edges of the dorsal sclerite of the first thoracic segment. Based on the specific structure of the apparatus, we conclude that it was probably used by females to hold on to males during copulation. A defensive or prey-catching function appears less likely. A similar mechanism did not evolve in any other known known group of extant or extinct insects.