Single-copy nuclear genes resolve the phylogeny of the holometabolous insects

Background  

Evolutionary relationships among the 11 extant orders of insects that undergo complete metamorphosis, called Holometabola, remain either unresolved or contentious, but are extremely important as a context for accurate comparative biology of insect model organisms. The most phylogenetically enigmatic holometabolan insects are Strepsiptera or twisted wing parasites, whose evolutionary relationship to any other insect order is unconfirmed. They have been controversially proposed as the closest relatives of the flies, based on rDNA, and a possible homeotic transformation in the common ancestor of both groups that would make the reduced forewings of Strepsiptera homologous to the reduced hindwings of Diptera. Here we present evidence from nucleotide sequences of six single-copy nuclear protein coding genes used to reconstruct phylogenetic relationships and estimate evolutionary divergence times for all holometabolan orders.     

Insufficient resolving power of mitogenome data in deciphering deep phylogeny of Holometabola

The mitochondrial genome (mitogenome) is one of the most widely used markers for phylogenetic analysis. Compared with whole-genome data, mitogenome data are less expensive to obtain and easier to manipulate. However, compositional bias and accelerated evolutionary rate reduce the effectiveness of the mitogenome in determining insect phylogeny. This study shows that mitogenome data are not suitable to reconstruct deep holometabolan evolution, even with a most comprehensive data coding scheme and the more realistic CAT model. For the deep levels of divergence within Holometabola, protein-coding genes only retain weak phylogenetic signals, leading to peculiar interordinal relationships. Consensus relationships in the Holometabola phylogeny, such as the monophyly of Holometabola, the most basal position of Hymenoptera, and the sister group relationship between the Strepsiptera and Coleoptera were rarely resolved in our analyses. The relationships of the holometabolan groups as inferred by mitogenomes are highly vulnerable to gene types, data coding regimes, model choice, and optimality criteria, and no consistent alternative hypothesis of Holometabola's relationships is supported. Thus, we suggest that the slowly evolving nuclear genes or genome-scale approaches may be better options for resolving deep-level phylogeny of Holometabola.     

Mitochondrial genomes in the Hymenoptera and their utility as phylogenetic markers

Abstract.  In this study, we assessed the ability of mitochondrial genome sequences to recover a test phylogeny of five hymenopteran taxa from which phylogenetic relationships are well accepted. Our analyses indicated that the test phylogeny was well recovered in all nucleotide Bayesian analyses when all the available holometabolan (i.e. outgroup) taxa were included, but only in Bayesian analyses excluding third codon positions when only the hymenopteran representatives and a single outgroup were included. This result suggests that taxon sampling of the outgroup might be as important as taxon sampling of the ingroup when recovering hymenopteran phylogenetic relationships using whole mitochondrial genomes. Parsimony analyses were more sensitive to both taxon sampling and the analytical model than Bayesian analyses, and analyses using the protein dataset did not recover the test phylogeny. In general, mitochondrial genomes did not resolve the position of the Hymenoptera within the Holometabola with confidence, suggesting that an increased taxon sampling, both within the Holometabola and among outgroups, is necessary.     

Monophyletic Polyneoptera recovered by wing base structure

Phylogenetic relationships among the winged orders of Polyneoptera [Blattodea, Dermaptera, Embiodea (=Embioptera), Isoptera, Mantodea, Orthoptera, Phasmatodea, Plecoptera and Zoraptera] were estimated based on morphological data selected from the hindwing base structure. Cladistic analyses were carried out using hindwing base data alone and in combination with other, more general, morphological data. Both datasets resulted in similar trees and recovered the monophyly of Polyneoptera. Deepest phylogenetic relationships among the polyneopteran orders were not confidently estimated, but the monophyly of Mystroptera (= Embiodea + Zoraptera), Orthopterida (= Orthoptera + Phasmatodea) and Dictyoptera (= Blattodea + Mantodea + Isoptera) was supported consistently. In contrast, placements of Plecoptera and Dermaptera were unstable, although independent analysis of the wing base data supported their sister‐group relationship with two nonhomoplasious synapomorphies (unique conditions in the ventral basisubcostale, and in the articulation between the antemedian notal wing process and first axillary sclerite). Results from the combined wing base plus general morphology data were consistent, even if the wingless orders Grylloblattodea and Mantophasmatodea were included in the analysis. Generally, trees obtained from the present analyses were concordant with the results from other morphological and molecular analyses, but Isoptera were placed inappropriately to be the sister of Blattodea + Mantodea by the inclusion of the wing base data, probably as a result of morphological regressions of the order.     

Interrelationships and evolution of the tapeworms (Platyhelminthes: Cestoda)

Interrelationships of the tapeworms (Platyhelminthes: Cestoda) were examined by use of small (SSU) and large (LSU) subunit ribosomal DNA sequences and morphological characters. Fifty new complete SSU sequences were added to 21 sequences previously determined, and 71 new LSU (D1-D3) sequences were determined for the complementary set of taxa representing each of the major lineages of cestodes as currently understood. New sequences were determined for three amphilinidean taxa, but were removed from both alignments due to their excessively high degree of divergence from other cestode sequences. A morphological character matrix coded for supraspecific taxa was constructed by the modification of matrices from recently published studies. Maximum-parsimony (MP) analyses were performed on the LSU, SSU, LSU+SSU, and morphological data partitions, and minimum-evolution (ME) analyses utilizing a general time reversible model of nucleotide substitution including estimates of among-site rate heterogeneity were performed on the molecular data partitions. Resulting topologies were rooted at the node separating the Gyrocotylidea from the Eucestoda. The LSU data were found to be more informative than the SSU data and were more consistent with inferences from morphology, although nodal support was generally weak for most basal nodes. One class of transitions was found to be saturated for comparisons between the most distantly related taxa (gyrocotylideans vs cyclophyllideans and tetrabothriideans). Differences in the topologies resulting from MP and ME analyses were not statistically significant. Nonstrobilate orders formed the basal lineages of trees resulting from analysis of LSU data and morphology. Difossate orders were basal to tetrafossate orders, the latter of which formed a strongly supported clade. A clade including the orders Cyclophyllidea, Nippotaeniidea, and Tetrabothriidea was supported by all data partitions and methods of analysis. Paraphyly of the orders Pseudophyllidea, Tetraphyllidea, and Trypanorhyncha was consistent among the molecular data partitions. Inferences are made regarding a monozoic (nonsegmented) origin of the Eucestoda as represented by the Caryophyllidea and for the evolution of the strobilate and acetabulate/tetrafossate conditions having evolved in a stepwise pattern.     

Morphological disparity and evolutionary rates of cranial and postcranial characters in sloths (Mammalia,Pilosa, Folivora)

Sloth morphological evolution has been widely studied qualitatively, with comparative anatomy and morpho-functional approaches, or through quantitative assessments of morphological variation using morphometrics. Only recently, however, have folivoran morphological disparity and evolutionary rates begun to be evaluated using discrete character data. Nonetheless, patterns of morphological evolution in separate character partitions have not been investigated, neither the relative influence of, on the one hand, phylogeny, and on the other, dietary and locomotory adaptations of sloths. Here we evaluate those patterns using a phylomorphospace approach, quantifying morphological disparity and evolutionary rates, and investigating possible drivers of morphological evolution for cranial and postcranial characters in Folivora. The evolution of the morphology in those partitions is associated with distinct patterns of disparity among clades and ecological groups, even though the two partitions do not differ substantially in overall evolutionary tempo. Historical processes shaped the morphological evolution of sloths more consistently than ecological ones, although changes in postcranial characters also seem to be associated with locomotory adaptations, in which morphological convergences were much more common. We also discuss important methodological trade-offs in investigations of partitioned datasets mostly composed of fossil taxa.     

Aligned 18S and insect phylogeny

The nuclear small subunit rRNA (18S) has played a dominant role in the estimation of relationships among insect orders from molecular data. In previous studies, 18S sequences have been aligned by unadjusted automated approaches (computer alignments that are not manually readjusted), most recently with direct optimization (simultaneous alignment and tree building using a program called "POY"). Parsimony has been the principal optimality criterion. Given the problems associated with the alignment of rRNA, and the recent availability of the doublet model for the analysis of covarying sites using Bayesian MCMC analysis, a different approach is called for in the analysis of these data. In this paper, nucleotide sequence data from the 18S small subunit rRNA gene of insects are aligned manually with reference to secondary structure, and analyzed under Bayesian phylogenetic methods with both GTR+I+G and doublet models in MrBayes. A credible phylogeny of Insecta is recovered that is independent of the morphological data and (unlike many other analyses of 18S in insects) not contradictory to traditional ideas of insect ordinal relationships based on morphology. Hexapoda, including Collembola, are monophyletic. Paraneoptera are the sister taxon to a monophyletic Holometabola but weakly supported. Ephemeroptera are supported as the sister taxon of Neoptera, and this result is interpreted with respect to the evolution of direct sperm transfer and the evolution of flight. Many other relationships are well-supported but several taxa remain problematic, e.g., there is virtually no support for relationships among orthopteroid orders. A website is made available that provides aligned 18S data in formats that include structural symbols and Nexus formats.     

Insect phylogenomics: results, problems and the impact of matrix composition

In this study, we investigated the relationships among insect orders with a main focus on Polyneoptera (lower Neoptera: roaches, mantids, earwigs, grasshoppers, etc.), and Paraneoptera (thrips, lice, bugs in the wide sense). The relationships between and within these groups of insects are difficult to resolve because only few informative molecular and morphological characters are available. Here, we provide the first phylogenomic expressed sequence tags data ('EST': short sub-sequences from a c(opy) DNA sequence encoding for proteins) for stick insects (Phasmatodea) and webspinners (Embioptera) to complete published EST data. As recent EST datasets are characterized by a heterogeneous distribution of available genes across taxa, we use different rationales to optimize the data matrix composition. Our results suggest a monophyletic origin of Polyneoptera and Eumetabola (Paraneoptera + Holometabola). However, we identified artefacts of tree reconstruction (human louse Pediculus humanus assigned to Odonata (damselflies and dragonflies) or Holometabola (insects with a complete metamorphosis); mayfly genus Baetis nested within Neoptera), which were most probably rooted in a data matrix composition bias due to the inclusion of sequence data of entire proteomes. Until entire proteomes are available for each species in phylogenomic analyses, this potential pitfall should be carefully considered.     

Morphology and angiosperm systematics in the molecular era

Several ways in which morphology is used in systematic and evolutionary research in angiosperms are shown and illustrated with examples: 1) searches for special structural similarities, which can be used to find hints for hitherto unrecognized relationships in groups with unresolved phylogenetic position; 2) cladistic studies based on morphology and combined morphological and molecular analyses; 3) comparative morphological studies in new, morphologically puzzling clades derived from molecular studies; 4) studies of morphological character evolution, unusual evolutionary directions, and evolutionary lability based on molecular studies; and 5) studies of organ evolution. Conclusions: Goals of comparative morphology have shifted in the present molecular era. Morphology no longer plays the primary role in phylogenetic studies. However, new opportunities for morphology are opening up that were not present in the premolecular era: 1) phylogenetic studies with combined molecular and morphological analyses; 2) reconstruction of the evolution of morphological features based on molecularly derived cladograms; 3) refined analysis of morphological features induced by inconsistencies of previous molecular and molecular phylogenetic analyses; 4) better understanding of morphological features by judgment in a wider biological context; 5) increased potential for including fossils in morphological analyses; and 6) exploration of the evolution of morphological traits by integration of comparative structural and molecular developmental genetic aspects (Evo-Devo); this field is still in its infancy in botany; its advancement is one of the major goals of evolutionary botany.     

The role of character loss in phylogenetic reconstruction as exemplified for the Annelida

Annelid relationships are controversial, and molecular and morphological analyses provide incongruent estimates. Character loss is identified as a major confounding factor for phylogenetic analyses based on morphological data. A direct approach and an indirect approach for the identification of character loss are discussed. Character loss can frequently be found within annelids and examples of the loss of typical annelid characters, like chaetae, nuchal organs, coelomic cavities and other features, are given. A loss of segmentation is suggested for Sipuncula and Echiura; both are supported as annelid ingroups in molecular phylogenetic analyses. Moreover, character loss can be caused by some modes of heterochronic evolution (paedomorphosis) and, as shown for orbiniid and arenicolid polychaetes, paedomorphic taxa might be misplaced in phylogenies derived from morphology. Different approaches for dealing with character loss in cladistic analyses are discussed. Application of asymmetrical character state transformation costs or usage of a dynamic homology framework represents promising approaches. Identifying character loss prior to a phylogenetic analysis will help to refine morphological data matrices and improve phylogenetic analyses of annelid relationships.     

脉翅总目系统发育研究进展

脉翅总目是全变态类昆虫中起源较早的古老类群之一,有关该类群的分类及系统发育研究对阐明全变态类昆虫的起源演化具有重要意义。文章就脉翅总目的系统地位、目级阶元、科级阶元和属种级阶元的系统发育几个方面的研究进行综述,着重介绍近年来国内外取得的研究成果,其中包括基于形态和分子数据所得的最新系统发育假设。最后,对脉翅总目系统发育研究中尚未解决的主要问题进行归纳。     

Correlation with a limited set of behavioral niches explains the convergence of somatic morphology in mygalomorph spiders

Understanding the drivers of morphological convergence requires investigation into its relationship with behavior and niche space, and such investigations in turn provide insights into evolutionary dynamics, functional morphology, and life history. Mygalomorph spiders (trapdoor spiders and their kin) have long been associated with high levels of morphological homoplasy, and many convergent features can be intuitively associated with different behavioral niches. Using genus-level phylogenies based on recent genomic studies and a newly assembled matrix of discrete behavioral and somatic morphological characters, we reconstruct the evolution of burrowing behavior in the Mygalomorphae, compare the influence of behavior and evolutionary history on somatic morphology, and test hypotheses of correlated evolution between specific morphological features and behavior. Our results reveal the simplicity of the mygalomorph adaptive landscape, with opportunistic, web-building taxa at one end, and burrowing/nesting taxa with structurally modified burrow entrances (e.g., a trapdoor) at the other. Shifts in behavioral niche, in both directions, are common across the evolutionary history of the Mygalomorphae, and several major clades include taxa inhabiting both behavioral extremes. Somatic morphology is heavily influenced by behavior, with taxa inhabiting the same behavioral niche often more similar morphologically than more closely related but behaviorally divergent taxa, and we were able to identify a suite of 11 somatic features that show significant correlation with particular behaviors. We discuss these findings in light of the function of particular morphological features, niche dynamics within the Mygalomorphae, and constraints on the mygalomorph adaptive landscape relative to other spiders.     

Old trees, new trees--is there any progress?

The amount of comparative data for phylogenetic analyses is constantly increasing. Data come from different directions such as morphology, molecular genetics, developmental biology and paleontology. With the increasing diversity of data and of analytical tools, the number of competing hypotheses on phylogenetic relationships rises, too. The choice of the phylogenetic tree as a basis for the interpretation of new data is important, because different trees will support different evolutionary interpretations of the data investigated. I argue here that, although many problematic aspects exist, there are several phylogenetic relationships that are supported by the majority of analyses and may be regarded as something like a robust backbone. This accounts, for example, for the monophyly of Metazoa, Bilateria, Deuterostomia, Protostomia (= Gastroneuralia), Gnathifera, Spiralia, Trochozoa and Arthropoda and probably also for the branching order of diploblastic taxa (“Porifera”, Trichoplax adhaerens, Cnidaria and Ctenophora). Along this “backbone”, there are several problematic regions, where either monophyly is questionable and/or where taxa “rotate” in narrow regions of the tree. This is illustrated exemplified by the probable paraphyly of Porifera and the phylogenetic relationships of basal spiralian taxa. Two problems span wider regions of the tree: the position of Arthropoda either as the sister taxon of Annelida (= Articulata) or of Cycloneuralia (= Ecdysozoa) and the position of tentaculate taxa either as sister taxa of Deuterostomia (= Radialia) or within the taxon Spiralia. The backbone makes it possible to develop a basic understanding of the evolution of genes, molecules and structures in metazoan animals.     

Phylogeny and diversification of the true water bugs (Insecta: Hemiptera: Heteroptera: Nepomorpha)

Climate fluctuations and tectonic reconfigurations associated with environmental changes play large roles in determining patterns of adaptation and diversification, but studies documenting how such drivers have shaped the evolutionary history and diversification dynamics of limnic organisms during the Mesozoic are scarce. Members of the heteropteran infraorder Nepomorpha, or aquatic bugs, are ideal for testing the effects of these determinants on their diversification pulses because most species are confined to aquatic environments during their entire life. The group has a relatively mature taxonomy and is well represented in the fossil record. We investigated the evolution of Nepomorpha based on phylogenetic analyses of morphological and molecular characters sampled from 115 taxa representing all 13 families and approximately 40% of recognized genera. Our results were largely congruent with the phylogenetic relationships inferred from morphology. A divergence dating analysis indicated that Nepomorpha began to diversify in the late Permian (approximately 263 Ma), and diversification analyses suggested that palaeoecological opportunities probably promoted lineage diversification in this group.     

A priori assumptions about characters as a cause of incongruence between molecular and morphological hypotheses of primate interrelationships

When molecules and morphology produce incongruent hypotheses of primate interrelationships, the data are typically viewed as incompatible, and molecular hypotheses are often considered to be better indicators of phylogenetic history. However, it has been demonstrated that the choice of which taxa to include in cladistic analysis as well as assumptions about character weighting, character state transformation order, and outgroup choice all influence hypotheses of relationships and may positively influence tree topology, so that relationships between extant taxa are consistent with those found using molecular data. Thus, the source of incongruence between morphological and molecular trees may lie not in the morphological data themselves but in assumptions surrounding the ways characters evolve and their impact on cladistic analysis. In this study, we investigate the role that assumptions about character polarity and transformation order play in creating incongruence between primate phylogenies based on morphological data and those supported by multiple lines of molecular data. By releasing constraints imposed on published morphological analyses of primates from disparate clades and subjecting those data to parsimony analysis, we test the hypothesis that incongruence between morphology and molecules results from inherent flaws in morphological data. To quantify the difference between incongruent trees, we introduce a new method called branch slide distance (BSD). BSD mitigates many of the limitations attributed to other tree comparison methods, thus allowing for a more accurate measure of topological similarity. We find that releasing a priori constraints on character behavior often produces trees that are consistent with molecular trees. Case studies are presented that illustrate how congruence between molecules and unconstrained morphological data may provide insight into issues of polarity, transformation order, homology, and homoplasy.     

Permian parallelisms: Reanalysis of †Tshekardocoleidae sheds light on the earliest evolution of the Coleoptera

The Coleoptera provides an excellent example of the value of fossils for understanding the evolutionary patterns of recent lineages. We reevaluate the morphology of the Early Permian †Tshekardocoleidae to test alternative phylogenetic hypotheses relating to the Palaeozoic evolution of the order. We discuss prior interpretations and revise an earlier data matrix. Both Bayesian and parsimony analyses support the monophyly of Coleoptera excluding †Tshekardocoleidae (= Mesocoleoptera), and of Coleoptera excluding †Tshekardocoleidae and †Permocupedidae (= Metacoleoptera). Plesiomorphies preserved in †Tshekardocoleidae are elytra, which rest over the body in a loose tent-like manner, with flat lateral flanges, projecting beyond the abdominal apex, and abdomens that are flexible and nearly cylindrical. Apomorphies of Mesocoleoptera include shortening of the elytra and a closer fit with the flattened and probably more rigid abdomen. A crucial synapomorphy of Metacoleoptera is the tightly sealed subelytral space, which may have been advantageous during the Permian aridification. Taxon exclusion experiments show that †Tshekardocoleidae is crucial for understanding the early evolution of Coleoptera and that its omission strongly affects ancestral state polarities as well as topology, including crown-group taxa. By constraining the relationships of extant taxa to match those supported by phylogenomic analysis, we demonstrate that features shared by Archostemata with Permian stem groups are most reasonably supported as plesiomorphic and that the smooth and simplified body forms of Polyphaga, Adephaga, Myxophaga, and Micromalthidae were derived in parallel. Our study highlights the reciprocal illumination of molecular, morphological, and paleontological data, and paves the way for tip-dating analysis across the order.     

Key Innovations: Further Remarks on the Importance of Morphology in Elucidating Systematic Relationships and Adaptive Radiations

The present paper is an argument in support of the continued importance of morphological systematics and a plea for improving molecular phylogenetic analyses by addressing explicit character transformations. We use here the inference of key innovations and adaptive radiations to demonstrate why morphological systematics is still relevant and necessary. After establishing that theories of phylogenetic relationship offer robust explanatory bases for discussing evolutionary diversification, the following topics are addressed: (1) the inference of key innovations grounded in phylogenetic analyses; (2) the epistemic distinction between character ‘mapping’ and relevant evidence in systematic and evolutionary studies; and (3) key innovations in molecular phylogenetics. We emphasize that the discovery of key innovations, in fossil or extant taxa, further strengthens the importance of morphology in systematic and evolutionary inferences, as they reveal scenarios of character transformation that have led to asymmetrical sister-group diversification. Our main conclusion is that understanding characters in and of themselves, when properly contextualized systematically, is what evolutionary biologists should be concerned with, whereas the analysis of tree topology alone, in which statistical nodal support measures are the sole indicators of phylogenetic affinity, does not lead to a fuller understanding of key innovations.     

Phylogenetic implications of the morphology of the braincase of caecilian amphibians (Gymnophiona)

Caecilian morphology is strongly modified in association with their fossorial mode of life. Currently phylogenetic analyses of characters drawn from the morphology of caecilians lack resolution, as well as complementarity, with results of phylogenetic analyses that employ molecular data. Stemming from the hypothesis derived from the mammal literature that the braincase has the greatest potential (in comparison to other cranial units) to yield phylogenetic information, the braincase and intimately associated stapes of 27 species (23 genera) of extant caecilians were examined using images assembled via microcomputed tomography. Thirty‐four new morphological characters pertaining to the braincase and stapes were identified and tested for congruence with previously recognized morphological characters. The results reveal that when added to previous character matrices, characters of the braincase and stapes resolve generic‐level relationships in a way that is largely congruent with the results of molecular analyses. Analysis of a combined data set of molecular and morphological data provides a framework for conducting ancestral character state reconstructions, which resulted in the identification of 95 new synapomorphies for various clades and taxa, 27 of which appear to be unique for the taxa that possess them. Together these data demonstrate the utility of the application of characters of the braincase and stapes for resolving phylogenetic relationships for a group whose morphology is largely confounded by functional modifications. In addition this study provides evidence of the utility of the braincase in resolving problematic morphology‐based phylogeny outside of Amniota, in an amphibian group. © 2012 The Linnean Society of London, Zoological Journal of the Linnean Society, 2012, 166 , 160–201.