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 beetle superfamily Dytiscoidea, placed within the suborder Adephaga, comprises six families. The phylogenetic relationships of these families, whose species are aquatic, remain highly contentious. In particular the monophyly of the geographically disjunct Aspidytidae (China and South Africa) remains unclear. Here we use a phylogenomic approach to demonstrate that Aspidytidae are indeed monophyletic, as we inferred this phylogenetic relationship from analyzing nucleotide sequence data filtered for compositional heterogeneity and from analyzing amino-acid sequence data. Our analyses suggest that Aspidytidae are the sister group of Amphizoidae, although the support for this relationship is not unequivocal. A sister group relationship of Hygrobiidae to a clade comprising Amphizoidae, Aspidytidae, and Dytiscidae is supported by analyses in which model assumptions are violated the least. In general, we find that both concatenation and the applied coalescent method are sensitive to the effect of among-species compositional heterogeneity.Four-cluster likelihood-mapping suggests that despite the substantial size of the dataset and the use of advanced analytical methods, statistical support is weak for the inferred phylogenetic placement of Hygrobiidae. These results indicate that other kinds of data (e.g. genomic meta-characters) are possibly required to resolve the above-specified persisting phylogenetic uncertainties. Our study illustrates various data-driven confounding effects in phylogenetic reconstructions and highlights the need for careful monitoring of model violations prior to phylogenomic analysis. to coordination of taxon sampling and transcriptome sequencing. BM, DRM, MB, ON, RGB, and XZ, contributed to funding acquisition. DRM, DTB, FJ, HEE, KM, LH, MB, RSP, YA, and XZ collected samples and/or contributed to the data processing of the sequenced transcriptomes. AD, AV, JMP, LP, and SL performed the de novo transcriptome assembly and cross-contamination checks. AD, AV, and JMP performed the NCBI sequence submissions. AV, ON, and RMW performed the orthology inference and orthology assignment analyses. AV performed the phylogenetic analyses with contributions, suggestions and comments from BM, KM, and CM. AV, BM, ON, MB and RGB wrote the first draft of the manuscript, with AV taking the lead. All authors contributed with comments and suggestions on later versions of the manuscript. Declarations of interest: none Appendix A. Supplementary materialSupplementary data associated with this article can be found, in the online version, at (doi link upon acceptance). The filtered and unfiltered COGs as well as all inferred matrices and their partition files are available at the MENDELEY DATA repository (XXXXX).
BackgroundThe tribe Coccinellini is a group of relatively large ladybird beetles that exhibits remarkable morphological and biological diversity. Many species are aphidophagous, feeding as larvae and adults on aphids, but some species also feed on other hemipterous insects (i.e., heteropterans, psyllids, whiteflies), beetle and moth larvae, pollen, fungal spores, and even plant tissue. Several species are biological control agents or widespread invasive species (e.g., Harmonia axyridis (Pallas)). Despite the ecological importance of this tribe, relatively little is known about the phylogenetic relationships within it. The generic concepts within the tribe Coccinellini are unstable and do not reflect a natural classification, being largely based on regional revisions. This impedes the phylogenetic study of important traits of Coccinellidae at a global scale (e.g. the evolution of food preferences and biogeography).ResultsWe present the most comprehensive phylogenetic analysis of Coccinellini to date, based on three nuclear and one mitochondrial gene sequences of 38 taxa, which represent all major Coccinellini lineages. The phylogenetic reconstruction supports the monophyly of Coccinellini and its sister group relationship to Chilocorini. Within Coccinellini, three major clades were recovered that do not correspond to any previously recognised divisions, questioning the traditional differentiation between Halyziini, Discotomini, Tytthaspidini, and Singhikaliini. Ancestral state reconstructions of food preferences and morphological characters support the idea of aphidophagy being the ancestral state in Coccinellini. This indicates a transition from putative obligate scale feeders, as seen in the closely related Chilocorini, to more agile general predators.ConclusionsOur results suggest that the classification of Coccinellini has been misled by convergence in morphological traits. The evolutionary history of Coccinellini has been very dynamic in respect to changes in host preferences, involving multiple independent host switches from different insect orders to fungal spores and plants tissues. General predation on ephemeral aphids might have created an opportunity to easily adapt to mixed or specialised diets (e.g. obligate mycophagy, herbivory, predation on various hemipteroids or larvae of leaf beetles (Chrysomelidae)). The generally long-lived adults of Coccinellini can consume pollen and floral nectars, thereby surviving periods of low prey frequency. This capacity might have played a central role in the diversification history of Coccinellini.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-017-1002-3) contains supplementary material, which is available to authorized users.
Click-beetles (Coleoptera: Elateridae) are an abundant, diverse, and economically important beetle family that includes bioluminescent species. To date, molecular phylogenies have sampled relatively few taxa and genes, incompletely resolving subfamily level relationships. We present a novel probe set for anchored hybrid enrichment of 2260 single-copy orthologous genes in Elateroidea. Using these probes, we undertook the largest phylogenomic study of Elateroidea to date (99 Elateroidea, including 86 Elateridae, plus 5 non-elateroid outgroups). We sequenced specimens from 88 taxa to test the monophyly of families, subfamilies and tribes. Maximum likelihood and coalescent phylogenetic analyses produced well-resolved topologies. Notably, the included non-elaterid bioluminescent families (Lampyridae + Phengodidae + Rhagophthalmidae) form a clade within the otherwise monophyletic Elateridae, and Sinopyrophoridae may not warrant recognition as a family. All analyses recovered the elaterid subfamilies Elaterinae, Agrypninae, Cardiophorinae, Negastriinae, Pityobiinae, and Tetralobinae as monophyletic. Our results were conflicting on whether the hypnoidines are sister to Dendrometrinae or Cardiophorinae + Negastriinae. Moreover, we show that fossils with the eucnemid-type frons and elongate cylindrical shape may belong to Eucnemidae, Elateridae: Thylacosterninae, ancestral hard-bodied cantharoids or related extinct groups. Proposed taxonomic changes include recognition of Plastocerini as a tribe in Dendrometrinae and Hypnoidinae stat. nov. as a subfamily within Elateridae.
Phytophagous ladybird beetles of the tribe Epilachnini are a cosmopolitan, species-rich group of significant economic importance as pests of agricultural crops. The tribe is well characterized morphologically and clearly monophyletic, but very little is known about its internal phylogenetic relationships and their genus-level taxonomy. In order to infer the evolutionary history of Epilachnini, test its monophyly and provide a phylogeny-based classification, we assembled a comprehensive dataset, consisting of four DNA markers (18S and 28S rRNA and 16S, COI mtDNA) and a matrix of 104 morphological characters for 153 species of Epilachnini representing all previously recognised genera, ∼11% of the known species, and 14 outgroup taxa. Molecular, morphological and combined datasets were analysed using maximum likelihood, parsimony and Bayesian inference. Bayes factors and Approximately Unbiased tests (AU) were used to compare alternative phylogenetic hypotheses of unconstrained and backbone-constrained analysis.
Rove beetles of the tribe Quediini are abundant predators in humid microhabitats of forested, open, synanthropic or subterranean ecosystems, with just over 800 species distributed across the temperate and subtropical regions of the Northern Hemisphere. Previous molecular phylogenies included only a limited representation of this diversity but have already indicated that Quedius, containing the majority of Quediini species, is polyphyletic. Six genera, historically associated with Quediini but now Staphylininae incertae sedis, are known only from few pinned specimens and have never been sequenced. Recent synergy between target enrichment phylogenomics, low‐input sequencing of dry, pinned insect specimens and advances in alpha taxonomic knowledge have made comprehensive sampling of Quediini tractable. Here we developed a novel probe set specialized for anchored hybrid enrichment of 1229 single‐copy orthologous loci in Staphylinidae. In one of the largest target enrichment phylogenies of insects to‐date, we sequenced 201 ingroup taxa to clearly delimit monophyletic Quediini within Staphylininae and resolve relationships within this tribe, with 46% of sampled taxa derived from pinned specimens (0–45 years old). Maximum likelihood and coalescent phylogenetic analyses produced well‐resolved, congruent topologies that will serve as a framework for further exploration of this radiation and its necessary generic revision. The inclusion of nearly all remaining Staphylininae incertae sedis genera, all known only from pinned specimens, resulted in the creation of Quelaestrygonini Brunke, trib. n. and revised concepts for Cyrtoquediini and Indoquediini. Quediini was resolved as monophyletic with the transfer of Q. elevatus and Q. nigropolitus to other tribes but Quedius and its subgenera Microsaurus, Distichalius and Raphirus were shown to be para‐ or polyphyletic. Based on the results of our analyses, Velleiopsis Fairmaire, 1882 syn. n. and Megaquedius Casey, 1915 syn. n. are synonymized with Microsaurus Dejean, 1833 resulting in: Q. (Microsaurus) marginiventris (Fairmaire) comb. n., Q. (M.) varendorffi (Reitter) comb.n. Several species of Quedius were transferred from Microsaurus to Distichalius (Q. aethiops Smetana, Q. biann Smetana, Q. cingulatus Smetana and Q. taruni Smetana), Distichalius to Raphirus (Q. fagelianus Scheerpeltz) and Microsaurus to Raphirus (Q. mixtus Eppelsheim and Q. persicus Korge).
Cycads, unlike modern wind-pollinated conifers and Ginkgo, are unusual in that they are an ancient group of gymnosperms pollinated by insects [1-3]. Although it is well documented that cycads were diverse and abundant during the mid-Mesozoic, little is known about their biogeography and pollination before the rise of angiosperms. Direct fossil evidence illuminating the evolutionary history of cycads is extremely rare [4, 5]. Here we report a specialized beetle-mediated pollination mode from the mid-Cretaceous of Myanmar, wherein a new boganiid beetle, Cretoparacucujus cycadophilus, with specialized pollen-feeding adaptations in its mouthparts and legs, was associated with many pollen grains of Cycadopites. Phylogenetic analyses indicate Cretoparacucujus as a sister group to the extant Australian Paracucujus, which pollinate the cycad Macrozamia riedlei. Our discovery, along with the current disjunct distribution of related beetle-herbivore (tribe Paracucujini) and cycad-host (tribe Encephalarteae) pairs in South Africa and Australia, indicate a probable ancient origin of beetle pollination of cycads at least in the Early Jurassic, long before angiosperm dominance and the radiation of flowering-plant pollinators later in the Cretaceous.
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