Aphids (Hemiptera: Aphididae) are a lineage of ~5200 plant-feeding insects most abundant in temperate regions. The diversification of aphids is thought to be a rapid radiation, whereas abiotic and biotic factors heavily influence the morphologies. These factors have clouded the taxonomy at all taxonomic ranks, and the effect can be viewed in many incongruent molecular and morphological phylogenies. In this study, we address this problem using both genome and transcriptome data to estimate the phylogenomic relationships between 12 subfamilies with 48 ingroup taxa. We predicted a novel well-curated dataset of phylogenetically consistent orthologues that included 3162 genes to estimate a concatenated maximum likelihood and multi-species coalescent species trees. Our results suggest that there are three main clades of Aphididae subfamilies, which are congruent with a previous Sanger sequencing-based phylogenetic study. However, the relationship between the three clades of subfamilies is clouded by gene tree discordance, introgression and parent–child branches along the backbone that fall within the gene tree anomaly zone. In addition, our results suggest an introgression event between two agriculturally important species of aphids within the subfamily Aphidinae. Our research provides the first phylogenomic study of the Aphididae subfamilies and a foundation for future molecular and morphological studies into this adaptive radiation of insects.
Deep learning algorithms and particularly convolutional neural networks are very successful in pattern recognition from images and are increasingly employed in biology. The development of automated systems for rapid and reliable species identification is vital for insect systematics and may revolutionize this field soon. In this study, we demonstrate the ability of a convolutional neural network to identify species based on habitus photographs with expert-level accuracy in a taxonomically challenging group where a human-based identification would require notorious genitalia dissections. Using the economically important and polymorphic plant bug genus Adelphocoris Reuter (Heteroptera: Miridae) as a model group, we explore the variability in the performance of 11 convolutional neural models most commonly used for image classification, test the role of class-imbalance on the model performance assessment and visualize areas of interest using three interpretation algorithms. Classification performance in our experiments with collection-based habitus photographs is high enough to identify very similar species from a large group with an expert-level accuracy. The accuracy is getting lower only in the experiments with an additional dataset of Adelphocoris and other live plant bugs photographs taken from the Web. Our article demonstrates the importance of comprehensive institutional insect collections for bringing deep learning algorithms into service for systematic entomology using affordable equipment and methods.
We apply integrative taxonomy to solve a historical taxonomic impasse in a flat wasp group (Hymenoptera, Bethylidae). The phylogeny of Epyrinae is inferred with parsimony analyses under equal and implied weights, maximum likelihood and Bayesian inference using the nuclear markers 18S and 28S, the mitochondrial genes 16S, cytochrome oxidase subunit I and cytochrome B and 232 morphological characters. This is the first phylogenetic study to examine all 42 epyrine genera, including junior synonyms and extinct taxa, applying a combined molecular and morphological approach. This study considered 186 terminal taxa with 166 representing the ingroup taxa and 20 outgroup taxa. All resulting trees of the combined analyses recovered Anisepyris Kieffer, Aspidepyris Evans, Bakeriella Kieffer, Disepyris Kieffer, Laelius Ashmead and Trachepyris Kieffer as monophyletic; Chlorepyris Kieffer, Epyris Westwood, Formosiepyris Terayama and Holepyris Kieffer are non-monophyletic. Calyozina Enderlein is recovered as an independent lineage in implied weights, Bayesian and maximum likelihood topologies. Here, we describe three new genera and revalidate six genera, five of them junior synonyms of Epyris and one of Holepyris. In addition, we analysed the presence/absence of a sulcus between the mesoscuto-scutellar foveae and the shape of mesoscuto-scutellar foveae as the most important taxonomic characters for Epyrinae using ancestral state reconstruction. Finally, we provide a checklist of all species of Epyrinae, compiled via direct observation of the type, illustrations, or literature and an updated and illustrated taxonomic key for all epyrine genera.
We propose a higher classification of the lycaenid hairstreak tribe Eumaeini – one of the youngest and most species-rich butterfly tribes – based on autosome, Lepidopteran Z sex chromosome and mitochondrial protein-coding genes. The subtribe Neolycaenina Korb is a synonym of Callophryidina Tutt and subtribe Tmolusina Bálint is a synonym of Strephonotina K. Johnson, Austin, Le Crom, & Salazar. Proposed names are Rhammina Prieto & Busby, new subtribe; Timaetina Busby & Prieto, new subtribe; Atlidina Martins & Duarte, new subtribe; Evenina Faynel & Grishin, new subtribe; Jantheclina Robbins & Faynel, new subtribe; Paiwarriina Lamas & Robbins, new subtribe; Cupatheclina Lamas & Grishin, new subtribe; Parrhasiina Busby & Robbins, new subtribe; Ipideclina Martins & Grishin, new subtribe; and Trichonidina Duarte & Faynel, new subtribe. Phylogenetic results from the autosome and Z sex chromosome analyses are similar. Future analyses of datasets with hundreds of terminal taxa may be more practical time-wise by focussing on the smaller number of sex chromosome sequences (2.6% of nuclear protein-coding sequences). The phylogenetic classification and biological summaries for each subtribe suggest that a variety of factors affected Eumaeini diversification. About a dozen kinds of male secondary sexual organs with frequent evolutionary gains and losses occur in Atlidina, Evenina and Jantheclina (141 species combined). Females have been shown to use these organs to discriminate between conspecific and nonconspecific males, facilitating sympatry among close relatives. Eumaeina, Rhammina and Timaetina (140 species combined) are overwhelmingly montane with some evidence for a higher incidence of sympatric diversification. Seven Neotropical lineages in five subtribes invaded the temperate parts of the Nearctic Region with a diversification increase in the Callophryidina (262 species). North American Satyrium and Callophrys then invaded the Palearctic at least once each, with a major species-richness increase in Satyrium. The evolution of litter-feeding detritivores within Calycopidina (172 species) resulted in an increase in diversification rate compared with its flower-feeding sister lineage. Atlidina, Strephonotina, Parrhasiina and Strymonina (562 species combined) each contain a mixture of genera that specialize on one or two caterpillar food plant families and genera that are polyphagous. These would be appropriate subtribes to assess how the breadth of caterpillar food plants and the frequency of host shifts affected diversification.
We analysed a phylogenomic dataset comprising 730 terminal taxa and >160,000 nucleotide positions obtained using anchored hybrid enrichment of genomic DNA for a sample of deltocephaline leafhoppers and outgroups. Maximum likelihood analyses of concatenated nucleotide and amino acid sequences as well as coalescent gene tree analysis, yielded well-resolved phylogenetic estimates that were highly congruent with most branches receiving maximum support. Some topological incongruence occurs among the trees resulting from different analyses, mainly distributed among very short branches at intermediate levels in the phylogeny, pertaining to relationships among some tribes and multi-tribe lineages restricted to particular continents. Coalescent gene tree analysis revealed extensive gene tree conflict at these nodes, suggesting that certain relationships may remain difficult to resolve consistently even with genome-scale datasets and dense taxon sampling. Ancestral character state reconstruction of feeding preference indicates that grass specialization has been acquired three or fewer times in some highly diverse but relatively derived lineages. Molecular divergence time estimation suggests that the earliest divergences in the subfamily occurred during the Cretaceous but that most modern tribes did not appear until after the Cretaceous–Palaeogene boundary and that grass specialist lineages generally diversified and spread at the same time as grasslands were becoming widespread globally. These analyses also show a high level of global biogeographic structure, with several large lineages of primarily arboreal deltocephalines restricted to particular regions or continents and long-distance dispersal among continents occurring primarily among grass-specialist lineages. The results represent a major improvement over previous analyses of this diverse subfamily, which were based on 152 or fewer taxa and data from morphology and partial sequences of two genes.
Many phoretic relationships between arthropods are understudied because of taxonomic impediments. We here illustrate for avian lice riding on hippoboscid flies how new natural history data on phoretic relationships can be acquired quickly with modern and cost-effective barcoding techniques. Most avian lice are host-specific, but some can arrive on new hosts by hitchhiking on hippoboscid flies that feed on bird blood. Our summary of the literature yielded 254 published records which we here show to belong to two large and 13 small interaction networks for birds, flies, and lice. In order to generate new records, we developed a protocol based on screening bird carcasses sourced with the help of citizen scientists. The inspection of 131 carcasses from Singapore led to the first record of a Guimaraesiella Eichler (Ischnocera: Philopteridae) louse species riding on Ornithoica momiyamai Kishida flies collected from a pitta carcass. Phoresy may explain why this louse species is now known from three phylogenetically disparate hosts (Pitta moluccensis (Müller), Ficedula zanthopygia (Hay); Pardaliparus elegans Lesson). A second new case of phoresy enhanced a large interaction network dominated by Ornithophila metallica (Schiner), a cosmopolitan and polyphagous hippoboscid fly species. Overall, we argue that many two- and three-way phoretic relationships between arthropods (e.g., mites, pseudoscorpions, beetles, flies) can be resolved with cost-effective large-scale NGS barcoding, which can be used to partially overcome taxonomic impediments by pre-sorting specimens for taxonomic revision.
Mealybugs (Hemiptera: Pseudococcidae, Rhizoecidae and Xenococcidae) are important organisms for understanding processes of evolution, especially microbial symbiotic systems and interactions with host plants. Molecular phylogenetic trees were reconstructed for 128 species of mealybug using DNA fragments of eight loci, namely a mitochondrial (COI), nuclear ribosomal RNA (18S and 28S D2 and D10) and nuclear protein-encoding genes (EF-1α 5′ and 3′, Dynamin and wingless). In addition, data on the types of obligate endosymbionts were used to test the monophyly of major groups resulting from this molecular phylogeny. Based on the data from DNA sequences, morphology and obligate endosymbionts, we present a phylogeny supporting the families Rhizoecidae and Xenococcidae separate from Pseudococcidae, and the separation of Rastrococcus Ferris from Phenacoccinae and Pseudococcinae. Consequently, Rastrococcus is excluded from Phenacoccinae and elevated to subfamily Rastrococcinae subfam. nov. We also found support for Putoidae as a family distinct from the true mealybugs. Phenacoccus rubicola Kwon, Danzig & Park is transferred to Coccura Šulc.
The genus Thalpomena Saussure comprises nine species and four subspecies and is largely endemic to the Atlas Mountains (North Africa). Here, we used an evolutionary taxonomic approach to differentiate the species of the genus Thalpomena and to reconstruct their biogeographic history. Phylogenetic tree reconstruction based on five molecular markers revealed four distinct clades within the genus Thalpomena. These are not fully in line with the current taxonomy but rather seem to represent lineages defined by their distribution and hind wing banding patterns. All lineages are geographically separated and can be distinguished based on genetic, morphometric and ecological modelling data. Ancestral area reconstruction suggests an origin of the species in the southern regions of the Atlas Mountains (High Atlas to Aures Mountains). Molecular clock analysis promotes the glacial refugia theory, supporting the origin of Thalpomena in the Pliocene, followed by diversification events in the Pleistocene.