Conversion of forewings into hardened covers, elytra, was a ground-breaking morphological adaptation that has contributed to the extraordinary evolutionary success of beetles. Nevertheless, the ...knowledge of the functional aspects of these structures is still fragmentary and scattered across a large number of studies. Here, we have synthesized the presently available information on the evolution, development, modifications and biological functions of this crucial evolutionary novelty. The formation of elytra took place in the earliest evolution of Coleoptera, very likely already in the Carboniferous, and was achieved through the gradual process of progressive forewing sclerotization and the formation of inward directed epipleura and a secluded sub-elytral space. In many lineages of modern beetles, the elytra have been distinctly modified. This includes multiple surface modifications, a rigid connection or fusion of the elytra, or partial or complete reduction. Beetle elytra can be involved in a very broad spectrum of functions: mechanical protection of hind wings and body, anti-predator strategies, thermoregulation and water saving, water harvesting, flight, hind wing folding, diving and swimming, self-cleaning and burrow cleaning, phoresy of symbiotic organisms, mating and courtship, and acoustic communication. We postulate that the potential of the elytra to take over multiple tasks has enormously contributed to the unparalleled diversification of beetles.
The evolution and genomic basis of beetle diversity McKenna, Duane D.; Shin, Seunggwan; Ahrens, Dirk ...
Proceedings of the National Academy of Sciences - PNAS,
12/2019, Letnik:
116, Številka:
49
Journal Article
Recenzirano
Odprti dostop
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.
The phylogeny of insects, one of the most spectacular radiations of life on earth, has received considerable attention 1–3. However, the evolutionary roots of one intriguing group of insects, the ...twisted-wing parasites (Strepsiptera), remain unclear despite centuries of study and debate 1, 2, 4–11. Strepsiptera exhibit exceptional larval developmental features, consistent with a predicted step from direct (hemimetabolous) larval development to complete metamorphosis that could have set the stage for the spectacular radiation of metamorphic (holometabolous) insects 1, 12, 13. Here we report the sequencing of a Strepsiptera genome and show that the analysis of sequence-based genomic data (comprising more than 18 million nucleotides from nearly 4,500 genes obtained from a total of 13 insect genomes), along with genomic metacharacters, clarifies the phylogenetic origin of Strepsiptera and sheds light on the evolution of holometabolous insect development. Our results provide overwhelming support for Strepsiptera as the closest living relatives of beetles (Coleoptera). They demonstrate that the larval developmental features of Strepsiptera, reminiscent of those of hemimetabolous insects, are the result of convergence. Our analyses solve the long-standing enigma of the evolutionary roots of Strepsiptera and reveal that the holometabolous mode of insect development is more malleable than previously thought.
► First sequenced genome of a twisted-wing parasite (Insecta: Strepsiptera) ► Largest data set ever compiled for inferring the phylogenetic origin of Strepsiptera ► Strepsiptera are the closest living relatives of beetles (Coleoptera) ► Strepsiptera are not the “missing link” between hemi- and holometabolous insects
The morphology of mature larvae of Sisyra nigra was studied and documented with a broad spectrum of techniques. Special emphasis is on the cephalic anatomy and on the digestive tract. Cephalic ...structures are highly modified, with numerous autapomorphic conditions, including a globular head capsule, an extended area with large cornea lenses, a massive tentorium, a strongly developed prepharyngeal pumping apparatus with a horizontal arrangement of dilators, a sharp bend between the prepharynx and pharynx, and an unusual filter apparatus at the entrance of the large crop. The thoracic and abdominal muscle sets, and the legs are largely unmodified. Postcephalic apomorphies are conspicuous tergal setiferous tubercles, trifid setiferous pleural projections, single pretarsal claws, zigzag‐shaped abdominal tracheal gills, and a dense vestiture of setae on the terminal abdominal segments. Mandibulo‐maxillary stylets curved outwards are an unusual apomorphy also found in the semiaquatic larvae of Osmylidae. Semiaquatic or aquatic habits and secondarily multisegmented antennae are potential synapomorphies of these two groups and Nevrorthidae (Osmyloidea). A sistergroup relationship between Sisyridae and Nevrorthidae suggests that fully aquatic habits of larvae may be a synapomorphy of both families. A specialized terminal antennal seta is a potential groundplan apomorphy of Neuroptera, with secondary loss in Nevrorthidae and Ithonidae + Myrmeleontiformia, respectively. A trumpet‐shaped empodium is likely an apomorphy of Neuroptera excluding Coniopterygidae and Osmyloidea, and the secondary loss an apomorphy of Ithonidae on one hand, and Myrmeleontiformia excl. Psychopsidae on the other.
• Sisyridae evolved a unique association of larvae with freshwater sponges • Correlated apomorphies are a strongly developed prepharyngeal pump, loss of poison glands, and zig‐zag shaped abdominal tracheal gills • A new scenario for the evolution of larval features in Neuroptera is suggested
Despite considerable progress in systematics, a comprehensive scenario of the evolution of phenotypic characters in the mega-diverse Holometabola based on a solid phylogenetic hypothesis was still ...missing. We addressed this issue by de novo sequencing transcriptome libraries of representatives of all orders of holometabolan insects (13 species in total) and by using a previously published extensive morphological dataset. We tested competing phylogenetic hypotheses by analyzing various specifically designed sets of amino acid sequence data, using maximum likelihood (ML) based tree inference and Four-cluster Likelihood Mapping (FcLM). By maximum parsimony-based mapping of the morphological data on the phylogenetic relationships we traced evolutionary transformations at the phenotypic level and reconstructed the groundplan of Holometabola and of selected subgroups.
In our analysis of the amino acid sequence data of 1,343 single-copy orthologous genes, Hymenoptera are placed as sister group to all remaining holometabolan orders, i.e., to a clade Aparaglossata, comprising two monophyletic subunits Mecopterida (Amphiesmenoptera + Antliophora) and Neuropteroidea (Neuropterida + Coleopterida). The monophyly of Coleopterida (Coleoptera and Strepsiptera) remains ambiguous in the analyses of the transcriptome data, but appears likely based on the morphological data. Highly supported relationships within Neuropterida and Antliophora are Raphidioptera + (Neuroptera + monophyletic Megaloptera), and Diptera + (Siphonaptera + Mecoptera). ML tree inference and FcLM yielded largely congruent results. However, FcLM, which was applied here for the first time to large phylogenomic supermatrices, displayed additional signal in the datasets that was not identified in the ML trees.
Our phylogenetic results imply that an orthognathous larva belongs to the groundplan of Holometabola, with compound eyes and well-developed thoracic legs, externally feeding on plants or fungi. Ancestral larvae of Aparaglossata were prognathous, equipped with single larval eyes (stemmata), and possibly agile and predacious. Ancestral holometabolan adults likely resembled in their morphology the groundplan of adult neopteran insects. Within Aparaglossata, the adult's flight apparatus and ovipositor underwent strong modifications. We show that the combination of well-resolved phylogenies obtained by phylogenomic analyses and well-documented extensive morphological datasets is an appropriate basis for reconstructing complex morphological transformations and for the inference of evolutionary histories.
Celotno besedilo
Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
The Triassic was a crucial period for the early evolution and diversification of insects, including Coleoptera1–3—the most diverse order of organisms on Earth. The study of Triassic beetles, however, ...relies almost exclusively on flattened fossils with limited character preservation. Using synchrotron microtomography, we investigated a fragmentary Upper Triassic coprolite, which contains a rich record of 3D-preserved minute beetle remains of Triamyxa coprolithica gen. et sp. nov. Some specimens are nearly complete, preserving delicate structures of the legs and antennae. Most of them are congruent morphologically, implying that they are conspecific. Phylogenetic analyses suggest that T. coprolithica is a member of Myxophaga, a small suborder of beetles with a sparse fossil record, and that it represents the only member of the extinct family Triamyxidae fam. nov. Our findings highlight that coprolites can contain insect remains, which are almost as well preserved as in amber. They are thus an important source of information for exploring insect evolution before the Cretaceous-Neogene “amber time window.” Treated as food residues, insect remains preserved in coprolites also have important implications for the paleoecology of insectivores, in this case, likely the dinosauriform Silesaurus opolensis.
•The beetle Triamyxa coprolithica is described from a Triassic coprolite•It represents the only member of the extinct myxophagan family Triamyxidae•The coprolite was likely produced by the dinosauriform Silesaurus opolensis•The beetle fossils parallel younger amber inclusions in preservation quality
Qvarnström et al. use synchrotron microtomography to describe 3D-preserved beetle fossils from a Triassic coprolite. Most specimens belong to the new beetle Triamyxa coprolithica, which represents the only member of the extinct myxophagan family Triamyxidae. The fossil dropping was likely produced by the dinosauriform Silesaurus opolensis.
The latest advancements in DNA sequencing technologies have facilitated the resolution of the phylogeny of insects, yet parts of the tree of Holometabola remain unresolved. The phylogeny of ...Neuropterida has been extensively studied, but no strong consensus exists concerning the phylogenetic relationships within the order Neuroptera. Here, we assembled a novel transcriptomic dataset to address previously unresolved issues in the phylogeny of Neuropterida and to infer divergence times within the group. We tested the robustness of our phylogenetic estimates by comparing summary coalescent and concatenation-based phylogenetic approaches and by employing different quartet-based measures of phylogenomic incongruence, combined with data permutations.
Our results suggest that the order Raphidioptera is sister to Neuroptera + Megaloptera. Coniopterygidae is inferred as sister to all remaining neuropteran families suggesting that larval cryptonephry could be a ground plan feature of Neuroptera. A clade that includes Nevrorthidae, Osmylidae, and Sisyridae (i.e. Osmyloidea) is inferred as sister to all other Neuroptera except Coniopterygidae, and Dilaridae is placed as sister to all remaining neuropteran families. Ithonidae is inferred as the sister group of monophyletic Myrmeleontiformia. The phylogenetic affinities of Chrysopidae and Hemerobiidae were dependent on the data type analyzed, and quartet-based analyses showed only weak support for the placement of Hemerobiidae as sister to Ithonidae + Myrmeleontiformia. Our molecular dating analyses suggest that most families of Neuropterida started to diversify in the Jurassic and our ancestral character state reconstructions suggest a primarily terrestrial environment of the larvae of Neuropterida and Neuroptera.
Our extensive phylogenomic analyses consolidate several key aspects in the backbone phylogeny of Neuropterida, such as the basal placement of Coniopterygidae within Neuroptera and the monophyly of Osmyloidea. Furthermore, they provide new insights into the timing of diversification of Neuropterida. Despite the vast amount of analyzed molecular data, we found that certain nodes in the tree of Neuroptera are not robustly resolved. Therefore, we emphasize the importance of integrating the results of morphological analyses with those of sequence-based phylogenomics. We also suggest that comparative analyses of genomic meta-characters should be incorporated into future phylogenomic studies of Neuropterida.
Celotno besedilo
Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Abstract
Traumatic insemination refers to mating in which males pierce the female’s integument with his penis for insemination. Strepsiptera are often listed as an example for this mode of ...copulation. However, while traumatic insemination in Mengenillidae with free-living females is undisputed, its occurrence in Stylopidia with permanent endoparasitic females – 97% of the known species of Strepsiptera – has remained unclear. Rather, observations from a single study on Xenos vesparum (Xenidae) that questioned traumatic insemination in this species became generalized for Stylopidia. Here we show that integration of data from various imaging methods provides convincing evidence for traumatic insemination being phylogenetically widespread in Strepsiptera. Specifically, we provide the first evidence of injury wounds from traumatic insemination in species of Mengenillidae, Corioxenidae, Elenchidae, Halictophagidae and Xenidae. Using three-dimensional models of copulating pairs of Stylops ovinae (Stylopidae) and X. vesparum, we visualize the physical piercing of the female’s integument by the male’s penis. Finally, we show in species of Mengenillidae, Xenidae and Stylopidae that traumatic mating is associated with the injection of sperm in the female’s haemocoel. Our results significantly alter the understanding of the reproductive biology of Strepsiptera and imply that traumatic insemination has been the ancestral mode of copulation and retained in most, if not all, extant families.
Polyandry, the practice of females mating with multiple males, is a strategy found in many insect groups. Whether it increases the likelihood of receiving beneficial genes from male partners and ...other potential benefits for females is controversial. Strepsiptera are generally considered monandrous, but in a few species females have been observed copulating serially with multiple males. Here we show that the offspring of a single female can have multiple fathers in two Strepsiptera species: Stylops ovinae (Stylopidae) and Xenos vesparum (Xenidae). We studied female polyandry in natural populations of these two species by analysis of polymorphic microsatellite loci. Our results showed that several fathers can be involved in both species, in some cases up to four. Mating experiments with S. ovinae have shown that the first male to mates with a given female contributes to a higher percentage of the offspring than subsequent males. In X. vesparum, however, we found no significant correlation between mating duration and offspring contribution. The prolonged copulation observed in S. ovinae may have the advantage of reducing competition with sperm from other males. Our results show that monandry may not be the general pattern of reproduction in the insect order Strepsiptera.
Despite the ecological significance of ants and the intensive research attention they have received, thorough treatments of the anatomy and functional morphology are still scarce. In this study we ...document the head morphology of workers of the myrmicine Wasmannia affinis with optical microscopy, μ-computed tomography, scanning electron microscopy, and 3D reconstruction, providing the first complete anatomical treatment of an ant head with a broad array of modern techniques. We discuss the potential of the applied methods to generate detailed and well-documented morphological data sets with increased efficiency. We also address homology problems, particularly in the context of the cephalic digestive tract. According to our analyses the “pharynx” of previous ant studies is homologous to the prepharynx of other insects. We also discuss the phylogenetic potential and functional significance of the observed characters, with internal features such as tentorium and musculature discussed for the first time. Our investigation underlines that detailed anatomical data for Formicidae are still very fragmentary, which in turn limits our understanding of the major design elements underlying the ant bauplan. We attempt to provide a template for further anatomical studies, which will help to understand the evolution of this fascinating group on the phenotypic level.
•First modern documentation of the head anatomy of an ant worker.•Homology problems solved, particularly of the cephalic digestive tract.•Optimized workflow for acquisition and documentation of anatomical data.•Template for future work on ant cephalic anatomy.
PDF
