Genomic and Morphological Evidence Converge to Resolve the Enigma of Strepsiptera

Abstract

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.

1. Molecular phylogenetics and evolution of Coleoptera

“…Phylogenetic analyses of the resulting DNA sequence data from 14 insect genomes recovered a single maximally supported phylogenetic tree (100% ML bootstrap support, 1.00 Bayesian posterior probability support for all nodes) in which both Coleopterida ( Strepsiptera + Coleoptera) and Neuropteroidea (Neuropterida + Coleopterida) were monophyletic. These findings are fully consistent with Niehuis et al (2012).…”

“…A recent study of 13 insect genomes (Niehuis et al 2012) showed that Strepsiptera [represented by Mengenilla moldrzyki Pohl et al (Mengenillidae)] are not a subordinate group of beetles (represented by Priacma serrata (LeConte) (Cupedidae) and Tribolium castaneum (Herbst) (Tenebrionidae), which together span the basal split in Coleoptera) and that molecular and morphological data combined are consistent only with a sister group relationship between Strepsiptera and beetles, notably ruling out the possibility that Strepsiptera is a subordinate group of beetles. However, genome sequences from a neuropterid, which could verify this conclusion independent of morphological data, have so far been lacking.…”

“…To address these remaining possibilities using genomic data, I added unpublished sequences of 2549 genes (7,400,736 aligned nucleotide positions) from the genome of the neuropterid Chauliodes pectinicornis (Linnaeus) (Megaloptera: Corydalidae: Chauliodinae) 3 to the 13-genome data set of Niehuis et al (2012). Phylogenetic analyses of the resulting DNA sequence data from 14 insect genomes recovered a single maximally supported phylogenetic tree (100% ML bootstrap support, 1.00 Bayesian posterior probability support for all nodes) in which both Coleopterida ( Strepsiptera + Coleoptera) and Neuropteroidea (Neuropterida + Coleopterida) were monophyletic.…”

Species in Wolbachia? Proposal for the designation of ‘Candidatus Wolbachia bourtzisii’, ‘Candidatus Wolbachia onchocercicola’, ‘Candidatus Wolbachia blaxteri’, ‘Candidatus Wolbachia brugii’, ‘Candidatus Wolbachia taylori’, ‘Candidatus Wolbachia collembolicola’ and ‘Candidatus Wolbachia multihospitum’ for the different species within Wolbachia supergroups

“…For G + C content determination, contigs of each genome were concatenated, the number of G plus C nucleotides counted and the sum divided by the genome length. Genome of strain wMen was obtained from the Strepsiptera Genome Project [68], and genomes of strains wFol, wOc and wCte were only deposited like Sequence Read Archive (SRA) so they were not included in G + C determination because they were not completely sequenced [36].…”

A Diverse Paleobiota in Early Eocene Fushun Amber from China

“…A male twisted-winged parasite (Strepsiptera) has been recovered ( Figure 3G). Strepsiptera are an enigmatic order of minute entomophagous parasitoids whose phylogenetic affinities remain unclear, although they are probably related to beetles [31]. They are exceedingly rare in the fossil record, with Cenozoic fossils only in Eocene Baltic amber, Messel oil shale from Germany, and Miocene amber from the Dominican Republic [32].…”