Insect Phylogenomics: Exploring the Source of Incongruence Using New Transcriptomic Data (original) (raw)

Phylogenetic relationships among insect orders based on three nuclear protein-coding gene sequences

Molecular Phylogenetics and Evolution, 2011

Many attempts to resolve the phylogenetic relationships of higher groups of insects have been made based on both morphological and molecular evidence; nonetheless, most of the interordinal relationships of insects remain unclear or are controversial. As a new approach, in this study we sequenced three nuclear genes encoding the catalytic subunit of DNA polymerase delta and the two largest subunits of RNA polymerase II from all insect orders. The predicted amino acid sequences (In total, approx. 3500 amino acid sites) of these proteins were subjected to phylogenetic analyses based on the maximum likelihood and Bayesian analysis methods with various models. The resulting trees strongly support the monophyly of Palaeoptera, Neoptera, Polyneoptera, and Holometabola, while within Polyneoptera, the groupings of Isoptera/''Blattaria''/Mantodea (Superorder Dictyoptera), Dictyoptera/Zoraptera, Dermaptera/Plecoptera, Mantophasmatodea/Grylloblattodea, and Embioptera/Phasmatodea are supported. Although Paraneoptera is not supported as a monophyletic group, the grouping of Phthiraptera/Psocoptera is robustly supported. The interordinal relationships within Holometabola are well resolved and strongly supported that the order Hymenoptera is the sister lineage to all other holometabolous insects. The other orders of Holometabola are separated into two large groups, and the interordinal relationships of each group are (((Siphonaptera, Mecoptera), Diptera), (Trichoptera, Lepidoptera)) and ((Coleoptera, Strepsiptera), (Neuroptera, Raphidioptera, Megaloptera)). The sister relationship between Strepsiptera and Diptera are significantly rejected by all the statistical tests (AU, KH and wSH), while the affinity between Hymenoptera and Mecopterida are significantly rejected only by AU and KH tests. Our results show that the use of amino acid sequences of these three nuclear genes is an effective approach for resolving the relationships of higher groups of insects.

Progress, pitfalls and parallel universes: a history of insect phylogenetics

The phylogeny of insects has been both extensively studied and vigorously debated for over a century. A relatively accurate deep phylogeny had been produced by 1904. It was not substantially improved in topology until recently when phylogenomics settled many long-standing controversies. Intervening advances came instead through methodological improvement. Early molecular phylogenetic studies (1985–2005), dominated by a few genes, provided datasets that were too small to resolve controversial phylogenetic problems. Adding to the lack of consensus, this period was characterized by a polarization of philosophies, with individuals belonging to either parsimony or maximum-likelihood camps; each largely ignoring the insights of the other. The result was an unfortunate detour in which the few perceived phylogenetic revolutions published by both sides of the philosophical divide were probably erroneous. The size of datasets has been growing exponentially since the mid-1980s accompanied by a wave of confidence that all relationships will soon be known. However, large datasets create new challenges, and a large number of genes does not guarantee reliable results. If history is a guide, then the quality of conclusions will be determined by an improved understanding of both molecular and morphological evolution, and not simply the number of genes analysed.

Advances using molecular data in insect systematics

The size of molecular datasets has been growing exponentially since the mid 1980s, and new technologies have now dramatically increased the slope of this increase. New datasets include genomes, transcriptomes, and hybrid capture data, producing hundreds or thousands of loci. With these datasets, we are approaching a consensus on the higher level insect phylogeny. Huge datasets can produce new challenges in interpreting branch support, and new opportunities in developing better models and more sophisticated partitioning schemes. Dating analyses are improving as we recognize the importance of careful fossil calibration selection. With thousands of genes now available, coalescent methods have come of age. Barcode libraries continue to expand, and new methods are being developed for incorporating them into phylogenies with tens of thousands of individuals.

Advances in Insect Phylogeny at the Dawn of the Postgenomic Era

Annual Review of Entomology, 2012

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).

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

BMC Evolutionary Biology, 2014

Background: 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.

Phylogenomics resolves the timing and pattern of insect evolution

Science (New York, N.Y.), 2014

Insects are the most speciose group of animals, but the phylogenetic relationships of many major lineages remain unresolved. We inferred the phylogeny of insects from 1478 protein-coding genes. Phylogenomic analyses of nucleotide and amino acid sequences, with site-specific nucleotide or domain-specific amino acid substitution models, produced statistically robust and congruent results resolving previously controversial phylogenetic relations hips. We dated the origin of insects to the Early Ordovician [~479 million years ago (Ma)], of insect flight to the Early Devonian (~406 Ma), of major extant lineages to the Mississippian (~345 Ma), and the major diversification of holometabolous insects to the Early Cretaceous. Our phylogenomic study provides a comprehensive reliable scaffold for future comparative analyses of evolutionary innovations among insects.

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

BMC Biology, 2009

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 singlecopy nuclear protein coding genes used to reconstruct phylogenetic relationships and estimate evolutionary divergence times for all holometabolan orders.