Rolf G. Beutel

The Thoracic Morphology of Archostemata and the Relationships of the Extant Suborders of Coleoptera (Hexapoda)

Thoracic structures of Tetraphalerus bruchi are described in detail. The results were compared with features found in other representatives of Archostemata and other coleopteran suborders. Differences between thoracic structures of Tetraphalerus and members of other archostematan subgroups are discussed. External and internal characters of larval and adult representatives of 37 genera of the coleopteran suborders are outlined, coded and analysed cladistically, with four groups of Neuropterida as outgroup taxa. The results strongly suggest the branching pattern Archostemata + [Adephaga + (Myxophaga + Polyphaga)]. Coleoptera excluding Archostemata are supported with a high Bremer support. Important evolutionary changes linked with this branching event are simplifications of the thoracic skeleton resulting in reduced degrees of freedom (i.e. a restricted movability, especially at the leg bases), and a distinct simplification of the muscle system. This development culminates in Polyphaga, which are also strongly supported as a clade. Internalization of the partly reduced propleura, further muscle losses, and the fusion of the mesoventrites and metaventrites—with reversal in Scirtoidea and Derodontidae—are autapomorphies of Polyphaga. Archostemata is a small relict group in contrast to highly successful xylobiontic groups of Polyphaga. The less efficient thoracic locomotor apparatus, the lack of cryptonephric Malpighian tubules, and the rise of angiosperms with beetle groups primarily adjusted to them may have contributed to the decline of Archostemata.

Advances in Insect Phylogeny at the Dawn of the Postgenomic Era

Most species on Earth are insects and thus, understanding their evolutionary relationships is key to understanding the evolution of life. Insect relationships are increasingly well supported, due largely to technological advances in molecular sequencing and phylogenetic computational analysis. In this postgenomic era, insect systematics will be furthered best by integrative methods aimed at hypothesis corroboration from molecular, morphological, and paleontological evidence. This review of the current consensus of insect relationships provides a foundation for comparative study and offers a framework to evaluate incoming genomic evidence. Notable recent phylogenetic successes include the resolution of Holometabola, including the identification of the enigmatic Strepsiptera as a beetle relative and the early divergence of Hymenoptera; the recognition of hexapods as a crustacean lineage within Pancrustacea; and the elucidation of Dictyoptera orders, with termites placed as social cockroaches. Regions of the tree that require further investigation include the earliest winged insects (Palaeoptera) and Polyneoptera (orthopteroid lineages).

Phylogenetic Relationships of the Suborders of Coleoptera (Insecta)

One hundred seven external and internal characters of larval and adult representatives of 28 genera of the coleopteran suborders were analyzed cladistically. Four groups of Neuropterida were introduced as outgroup. The analysis yielded 18 trees with a minimum of 194 steps (CI 0.691). All trees support the monophyly of all four suborders and a branching pattern (Archostemata + (Adephaga + (Myxophaga + Polyphaga))). The presence of elytra with meso‐ and metathoracic locking devices, the specific hind‐wing folding, the close connection of exposed sclerites, the absence of the mera, the absence of eight thoracic muscles, the reduced abdominal sternite I, and the invagination of terminal segments are autapomorphies of Coleoptera. The monophyly of Coleoptera excl. Archostemata is supported by further transformations of the thoracic sclerites such as absence of the mesothoracic discriminal line and katepisternal joint, by an internalized or absent metathoracic trochantin, by the presence of a bending zone in the hind‐wing, and by eight further muscle losses. Fusion of tibia and tarsus and presence of a single claw are larval synapomorphies of Myxophaga and Polyphaga. Adults are characterized by fusion of protrochantin and propleura and by the rigid connection of the meso‐ and metathoracic ventrites. The eucinetoid lineage of Polyphaga is characterized by the secondary absence of the bending zone of the alae. This results in a distinctly simplified wing folding mechanism. The monophyly of Cucujiformia (+ Bostrichoidea) is supported by the presence of cryptonephric Malpighian tubules. Transformations of fore‐and hind‐wings, reinforcement and simplification of the thoracic exoskeleton, and an efficient use of a distinctly reduced set of thoracic muscles play an important role in the early evolution of Coleoptera. Many different larval character transformations take place in the earlier Mesozoic within the suborders.

The beetle tree of life reveals that Coleoptera survived end‐Permian mass extinction to diversify during the Cretaceous terrestrial revolution

Here we present a phylogeny of beetles (Insecta: Coleoptera) based on DNA sequence data from eight nuclear genes, including six single‐copy nuclear protein‐coding genes, for 367 species representing 172 of 183 extant families. Our results refine existing knowledge of relationships among major groups of beetles. Strepsiptera was confirmed as sister to Coleoptera and each of the suborders of Coleoptera was recovered as monophyletic. Interrelationships among the suborders, namely Polyphaga (Adephaga (Archostemata, Myxophaga)), in our study differ from previous studies. Adephaga comprised two clades corresponding to Hydradephaga and Geadephaga. The series and superfamilies of Polyphaga were mostly monophyletic. The traditional Cucujoidea were recovered in three distantly related clades. Lymexyloidea was recovered within Tenebrionoidea. Several of the series and superfamilies of Polyphaga received moderate to maximal clade support in most analyses, for example Buprestoidea, Chrysomeloidea, Coccinelloidea, Cucujiformia, Curculionoidea, Dascilloidea, Elateroidea, Histeroidea and Hydrophiloidea. However, many of the relationships within Polyphaga lacked compatible resolution under maximum‐likelihood and Bayesian inference, and/or lacked consistently strong nodal support. Overall, we recovered slightly younger estimated divergence times than previous studies for most groups of beetles. The ordinal split between Coleoptera and Strepsiptera was estimated to have occurred in the Early Permian. Crown Coleoptera appeared in the Late Permian, and only one or two lineages survived the end‐Permian mass extinction, with stem group representatives of all four suborders appearing by the end of the Triassic. The basal split in Polyphaga was estimated to have occurred in the Triassic, with the stem groups of most series and superfamilies originating during the Triassic or Jurassic. Most extant families of beetles were estimated to have Cretaceous origins. Overall, Coleoptera experienced an increase in diversification rate compared to the rest of Neuropteroidea. Furthermore, 10 family‐level clades, all in suborder Polyphaga, were identified as having experienced significant increases in diversification rate. These include most beetle species with phytophagous habits, but also several groups not typically or primarily associated with plants. Most of these groups originated in the Cretaceous, which is also when a majority of the most species‐rich beetle families first appeared. An additional 12 clades showed evidence for significant decreases in diversification rate. These clades are species‐poor in the Modern fauna, but collectively exhibit diverse trophic habits. The apparent success of beetles, as measured by species numbers, may result from their associations with widespread and diverse substrates – especially plants, but also including fungi, wood and leaf litter – but what facilitated these associations in the first place or has allowed these associations to flourish likely varies within and between lineages. Our results provide a uniquely well‐resolved temporal and phylogenetic framework for studying patterns of innovation and diversification in Coleoptera, and a foundation for further sampling and resolution of the beetle tree of life.

Structural Design and Biomechanics of Friction-Based Releasable Attachment Devices in Insects

Abstract Design of attachment devices in insects varies enormously in relation to different functional loads. Many systems, located on different parts of the body, involve surfaces with particular frictional properties. Such systems evolved to attach parts of the body to each other, or to attach an insect to the substratum by providing fast and reversible attachment/detachment. Among these systems, there are some that deal with predefined surfaces, and others, in which one surface remains unpredictable. The first type of system occurs, for example, in wing-locking devices and head-arresting systems and is called probabilistic fasteners. The second type is mainly represented by insect attachment pads of two alternative designs: hairy and smooth. The relationship between surface patterns and/or mechanical properties of materials of contact pairs results in two main working principles of the frictional devices: mechanical interlocking, or maximization of the contact area. We give an overview of the functional design of two main groups of friction-based attachment devices in insects: probabilistic fasteners and attachment pads.

Evolution of locomotory attachment pads of hexapods.

This study shows that, in their evolution, hexapods have convergently developed two distinctly different mechanisms to attach themselves to a variety of substrates during locomotion. The first mechanism is provided by hairy surfaces and the second one by smooth flexible pads. The main similarity of both mechanisms is that the structured pad surface or particular properties of pad materials guarantee a maximum real contact with diverse substrata, regardless of their microsculpture. Ten characters of the two alternative designs were coded and analyzed together with a data matrix containing 105 additional morphological characters of different stages and body parts. The analysis demonstrates that similar structures (arolium, euplantulae, hairy tarsomeres) have evolved independently in several hexapod lineages. The evolution of flight and the associated necessity of being able to cling to vegetation or other substrates are suggested to be major triggers for the evolution of attachment structures.

Morphological and molecular evidence converge upon a robust phylogeny of the megadiverse Holometabola

We present the largest morphological character set ever compiled for Holometabola. This was made possible through an optimized acquisition of data. Based on our analyses and recently published hypotheses based on molecular data, we discuss higher‐level phylogeny and evolutionary changes. We comment on the information content of different character systems and discuss the role of morphology in the age of phylogenomics. Microcomputer tomography in combination with other techniques proved highly efficient for acquiring and documenting morphological data. Detailed anatomical information (356 characters) is now available for 30 representatives of all holometabolan orders. A combination of traditional and novel techniques complemented each other and rapidly provided reliable data. In addition, our approach facilitates documenting the anatomy of model organisms. Our results show little congruence with studies based on rRNA, but confirm most clades retrieved in a recent study based on nuclear genes: Holometabola excluding Hymenoptera, Coleopterida (= Strepsiptera + Coleoptera), Neuropterida excl. Neuroptera, and Mecoptera. Mecopterida (= Antliophora + Amphiesmenoptera) was retrieved only in Bayesian analyses. All orders except Megaloptera are monophyletic. Problems in the analyses are caused by taxa with numerous autapomorphies and/or inapplicable character states due to the loss of major structures (such as wings). Different factors have contributed to the evolutionary success of various holometabolan lineages. It is likely that good flying performance, the ability to occupy different habitats as larvae and adults, parasitism, liquid feeding, and co‐evolution with flowering plants have played important roles. We argue that even in the “age of phylogenomics”, comparative morphology will still play a vital role. In addition, morphology is essential for reconstructing major evolutionary transformations at the phenotypic level, for testing evolutionary scenarios, and for placing fossil taxa.
© The Willi Hennig Society 2010.

The evolutionary history of holometabolous insects inferred from transcriptome-based phylogeny and comprehensive morphological data

BackgroundDespite 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.ResultsIn 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.ConclusionsOur 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.

Genomic and Morphological Evidence Converge to Resolve the Enigma of Strepsiptera

The phylogeny of insects, one of the most spectacular radiations of life on earth, has received considerable attention. However, the evolutionary roots of one intriguing group of insects, the twisted-wing parasites (Strepsiptera), remain unclear despite centuries of study and debate. 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. 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.

On the head morphology of Tetraphalerus, the phylogeny of Archostemata and the basal branching events in Coleoptera

Internal and external features of Tetraphalerus bruchi were studied using X‐ray microtomography (µ‐CT) and other techniques, and head structures were described in detail. µ‐Ct is highly efficient for the assessment of anatomical data. A data matrix with 90 morphological characters of recent and fossil beetles was analyzed with different approaches (parsimony, Bayesian analysis). The results of the parsimony analysis resulted in the following branching pattern: (†Tshekardocoleidae + (†Permocupedidae, †Rhombocoleidae + (†Triadocupedidae + ((Adephaga + (Myxophaga + Polyphaga))) + Archostemata s.str. [including Jurodidae]))). Sikhotealinia is placed as sister group of †Jurodes (Jurodidae), and Jurodidae as sister group of the remaining Archostemata (Bayesian analysis) or of a clade comprising Micromalthidae, Crowsoniellidae, †Ademosynidae, †Schizophoridae and †Catiniidae. The monophyly of Ommatidae and Cupedidae is well supported and Priacma is placed as the sister group of all other Cupedidae. Important events in the early evolution of Coleoptera are the shortening of the elytra and the transformation of the elytral venation (Coleoptera excluding †Tshekardocoleidae), the formation of a closed subelytral space (Coleoptera excluding †Tshekardocoleidae and †Permocupedidae), the reduction of two apical antennomeres, and the loss of the broad prothoracic postcoxal bridge (Coleoptera excluding †Tshekardocoleidae, †Permocupedidae and †Rhombocoleidae). Plesiomorphic features preserved in extant Archostemata are the tuberculate cuticle, the elytral pattern with parallel longitudinal ribs and window punctures, a mesoventrite with a transverse ridge, triangular mesocoxae with a distinct meron, and the exposed metatrochantin. The fossils included in the analyses do not only contribute to the reconstruction of character evolution but also influence the branching pattern. An understanding of the major evolutionary events in Coleoptera would not be possible without considering the rich fossil record of Permian and Mesozoic beetles.