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Misof, B.

Publications and source records attributed to Misof, B..

16 recordsLinked to original sources

Phylogenomics recovers multiple origins of portable case-making in caddisflies (Insecta: Trichoptera), the world's most common underwater architects

Caddisflies (Trichoptera) are among the most diverse groups of freshwater animals with more than 16,000 described species. They play an outsized role in freshwater ecology and environmental engineering in streams, rivers, and lakes. Because of this, they are frequently used as indicator organisms in biomonitoring programs. Despite their importance, key questions concerning the evolutionary history of caddisflies, such as the timing and origin of larval case-making, have been unanswered due to the lack of a well-resolved phylogenetic tree. To shed light on these questions in Trichoptera, we estimated a phylogenetic tree using a combination of transcriptomes and targeted enrichment data for 206 species, representing 48 of 52 extant families and 174 genera. We calibrated and dated the tree with a set of 33 carefully selected fossils. The first caddisflies originated in the Permian and the major suborders began to diversify in the Triassic. Ancestral state reconstruction and diversification analysis revealed that portable case-making evolved in three separate lineages and shifts in diversification occurred in concert with key evolutionary innovations other than case-making.

evolutionary biology↗

A transcriptome-based phylogeny of Scarabaeoidea confirms the sister group relationship of dung beetles and phytophagous pleurostict scarabs (Coleoptera)

Scarab beetles (Scarabaeidae) are a diverse and ecologically important group of angiosperm-associated insects. As conventionally understood, scarab beetles comprise two major lineages: dung beetles and the phytophagous Pleurosticti. However, previous phylogenetic analyses have not been able to convincingly answer the question whether or not the two lineages form a monophyletic group. Here we report our results from phylogenetic analyses of more than 4,000 genes mined from transcriptomes of more than 50 species of Scarabaeidae and other Scarabaeoidea. Our results provide convincing support for the monophyly of Scarabaeidae, confirming the debated sister group relationship of dung beetles and phytophagous pleurostict scarabs. Supermatrix-based maximum likelihood and multispecies coalescent phylogenetic analyses strongly imply the subfamily Melolonthinae as currently understood being paraphyletic. We consequently suggest various changes in the systematics of Melolonthinae: Sericinae Kirby, 1837 stat. rest. and sensu n. to include the tribes Sericini, Ablaberini and Diphucephalini, and Sericoidinae Erichson, 1847 stat. rest. and sensu n. to include the tribes Automoliini, Heteronychini, Liparetrini, Maechidiini, Scitalini, Sericoidini, and Phyllotocini. Both subfamilies appear to consistently form a monophyletic sister group to all remaining subfamilies so far included within pleurostict scarabs except Orphninae. Our results represent a major step towards understanding the diversification history of one of the largest angiosperm-associated radiations of beetles.

zoology↗

Contribution of hybridization to the evolution of a derived reproductive strategy in ricefishes

Transitions between reproductive strategies are costly and involve major changes in life history, behaviour and morphology. Nevertheless, in Sulawesi ricefishes, pelvic-brooding evolved from transfer-brooding in two distantly related lineages within in the genera Adrianichthys and in Oryzias, respectively. Females of pelvic-brooding species carry their eggs attached to their belly until the fry hatches. Despite their phylogenetic distance, both pelvic-brooding lineages share a set of external morphological traits. A recent study found no direct gene-flow between pelvic-brooding lineages suggesting independent evolution of the derived reproductive strategy. It could, however, also be more complex. Pre-existing variation in an admixed population may enable the re-use of genetic variants when subjected to similar external selection pressure, resulting in similar phenotypes. We thus used a multi-species coalescent (MSC) model and D-statistics to identify gene-tree - species-tree incongruencies, to evaluate the evolution of pelvic-brooding with respect to inter-specific gene-flow not only between pelvic-brooding lineages, but between pelvic-brooding lineages and other Sulawesi ricefish lineages. We found a general network-like evolution in Sulawesi ricefishes and as previously reported, no gene-flow between the pelvic-brooding lineages. Instead, we found hybridization between the ancestor of pelvic-brooding Oryzias and the common ancestor of the four Oryzias species from Lake Poso, home of the pelvic-brooding Adrianichthys lineage. Further, indications of introgression were located within two confidence intervals of quantitative trait loci (QTL) associated with pelvic-brooding in O. eversi. We thus hypothesize that a mix of de novo mutations and (ancient) standing genetic variation shaped the evolution of pelvic-brooding. Significance statementThe evolution of pelvic-brooding in Oryzias eversi (Beloniformes:Adrianichthyidae), was recently described to be independent from another pelvic-brooding ricefish lineage (Adrianichthys) from Sulawesi. We confirmed these results, and detected no gene flow between the two distantly related pelvic-brooding lineages. Instead, we found ancient gene flow from another Orzyias lineage into the pelvic-brooding Oryzias lineage. One of the previously described QTL for pelvic brooding overlaps with a region of high introgression signal. Therefore, we assume that not only de novo mutations contributed to the evolution of pelvic-brooding in Orzyias, but that introduced ancient genetic variation was likely also recruited for the evolution of this derived brooding strategy.

evolutionary biology↗

Intrasexual cuticular hydrocarbon dimorphism in a wasp sheds light on hydrocarbon biosynthesis genes in Hymenoptera

Cuticular hydrocarbons (CHCs) cover the cuticle of insects and serve as desiccation barrier and for chemical communication. While the main enzymatic steps of CHC biosynthesis are well understood, few of the underlying genes have been identified. Here we show how exploitation of intrasexual CHC dimorphism in a mason wasp, Odynerus spinipes, in combination with whole-genome sequencing and comparative transcriptomics facilitated identification of such genes. RNAi-mediated knockdown of twelve candidate gene orthologs in honey bees, Apis mellifera, confirmed nine genes impacting CHC profile composition. Most of them have predicted functions consistent with current knowledge of CHC metabolism. However, we found first-time evidence for a fatty acid amide hydrolase also influencing CHC profile composition. In situ hybridization experiments furthermore suggest trophocytes participating in CHC biosynthesis. Our results set the base for experimental CHC profile manipulation in Hymenoptera and imply that the evolutionary origin of CHC biosynthesis predates the arthropods colonization of land.

molecular biology↗

Standardized nuclear markers advance metazoan taxonomy

Species are the fundamental units of life and their recognition is essential for science and society. DNA barcoding, the use of a single and often mitochondrial gene, has been increasingly employed as a universal approach for the identification of animal species. However, this approach faces several challenges. Here, we demonstrate with empirical data from a number of metazoan animal lineages that multiple nuclear-encoded markers, so called universal single-copy orthologs (USCOs) performs much better than the single barcode gene to discriminate closely related species. Overcoming the general shortcomings of mitochondrial DNA barcodes, USCOs also accurately assign samples to higher taxonomic levels. These loci thus provide a powerful and unifying framework for species delimitation which considerably improves the DNA-based inference of animal species.

molecular biology↗

Dual targeting of salt inducible kinases and CSF1R uncouples bone formation and bone resorption

Bone formation and resorption are typically coupled, such that the efficacy of anabolic osteoporosis treatments may be limited by bone destruction. The multi-kinase inhibitor YKL-05-099 potently inhibits salt inducible kinases (SIKs) and may represent a promising new class of bone anabolic agents. Here we report that YKL-05-099 increases bone formation in hypogonadal female mice without increasing bone resorption. Postnatal mice with inducible, global deletion of SIK2 and SIK3 show increased bone mass, increased bone formation, and, distinct from the effects of YKL-05-099, increased bone resorption. No cell-intrinsic role of SIKs in osteoclasts was noted. In addition to blocking SIKs, YKL-05-099 also binds and inhibits CSF1R, the receptor for the osteoclastogenic cytokine M-CSF. Modeling reveals that YKL-05-099 binds to SIK2 and CSF1R in a similar manner. Dual targeting of SIK2/3 and CSF1R induces bone formation without concomitantly increasing bone resorption and thereby may overcome limitations of most current anabolic osteoporosis therapies.

physiology↗

Are fleas highly modified Mecoptera? Phylogenomic resolution of Antliophora (Insecta: Holometabola)

Insect orders have been defined and stable for decades, with few notable exceptions (e.g., Blattodea and Psocoptera). One of the few remaining questions of order-level monophyly is that of Mecoptera in respect to the phylogenetic placement of Siphonaptera (fleas). We used a large set of transcriptomic nucleotide sequence data representing 56 species and more than 3,000 single-copy genes to resolve the evolutionary history of Antliophora, including fleas (Siphonaptera), scorpionflies and relatives (Mecoptera), and true flies (Diptera). We find that fleas and mecopterans together are the sister group of flies. However, our data and/or analyses are unable to distinguish whether fleas are sister to a monophyletic Mecoptera, or whether they arose from within extant mecopteran families, rendering Mecoptera paraphyletic. We did not detect parameter bias in our dataset after applying a broad range of detection methods. Counter to a previous hypothesis that placed fleas within Mecoptera as the sister group to wingless boreids (snow fleas), we found a potential sister group relationship between fleas and the enigmatic family Nannochoristidae. Although we lack conclusive evidence, it seems possible that fleas represent the most-species rich group of modern mecopterans and that their parasitic lifestyle and morphological adaptations have simply made them unrecognizable in respect to their order-level classification.

evolutionary biology↗

How old are dragonflies and damselflies? Odonata (Insecta) transcriptomics resolve familial relationships

Dragonflies and damselflies, representing the insect order Odonata, are among the earliest flying insects with living (extant) representatives. However, unravelling details of their long evolutionary history, such as egg laying (oviposition) strategies, is impeded by unresolved phylogenetic relationships, an issue particularly prevalent in damselfly families and fossil lineages. Here we present the first transcriptome-based phylogenetic reconstruction of Odonata, analyzing 2,980 protein-coding genes in 105 species representing nearly all of the orders families (except Austropetaliidae and Neopetaliidae). All damselfly families and most dragonfly families are recovered as monophyletic groups. Our Molecular clock estimates suggest that crown-Zygoptera (damselflies) and -Anisoptera (dragonflies) both arose during the late Triassic. Several of the observed long inner branches in our topology are indicative of the extinction of once flourishing lineages. We also find that exophytic egg laying behaviour with a reduced ovipositor evolved in certain dragonflies during the late Jurassic / early Cretaceous. Lastly, we find that certain fossils have an unexpected deterring impact in divergence dating analysis.

evolutionary biology↗

Genomic signals of admixture and reinforcement between two closely related species of European sepsid flies

Interspecific gene flow by hybridization may weaken species barriers and adaptive divergence, but can also initiate reinforcement of reproductive isolation trough natural and sexual selection. The extent of interspecific gene flow and its consequences for the initiation and maintenance of species barriers in natural systems remain poorly understood, however. To assess genome-wide patterns of gene flow between the two closely related European dung fly species Sepsis cynipsea and Sepsis neocynipsea (Diptera: Sepsidae), we tested for historical gene flow with the aid of ABBA-BABA test using whole-genome resequencing data from pooled DNA of male specimens originating from natural and laboratory populations. We contrasted genome-wide variation in DNA sequence differences between samples from sympatric populations of the two species in France and Switzerland with that of interspecific differences between pairs of samples involving allopatric populations from Estonia and Italy. In the French Cevennes, we detected a relative excess of DNA sequence identity, suggesting interspecific gene flow in sympatry. In contrast, at two sites in Switzerland, we observed a relative depletion of DNA sequence identity compatible with reinforcement of species boundaries in sympatry. Our results suggest that the species boundaries between S. cynipsea and S. neocynipsea in Europe depend on the eco-geographic context.

evolutionary biology↗

A minimum reporting standard for multiple sequence alignments

Multiple sequence alignments (MSAs) play a pivotal role in studies of molecular sequence data, but nobody has developed a minimum reporting standard (MRS) to quantify the completeness of MSAs in terms of completely-specified nucleotides or amino acids. We present an MRS that relies on four simple completeness metrics. The metrics are implemented in AliStat, a program developed to support the MRS. A survey of published MSAs illustrates the benefits and unprecedented transparency offered by the MRS.

bioinformatics↗

Measuring historical and compositional signals in phylogenetic data

Most commonly-used molecular phylogenetic methods assume that the sequences evolved on a single bifurcating tree and that the evolutionary processes operating at the variable sites are Markovian. Typically, it is also assumed that these evolutionary processes were stationary, reversible and homogenous across the edges of the tree and that the multiple substitutions at variable sites occurred so infrequently that the historical signal (i.e., the signal in DNA that is due to the order and time of divergence event) in phylogenetic data has been retained, allowing for accurate phylogenetic estimates to be obtained from the data. Here, we present two metrics,{lambda} and{delta} CFS, to quantify the strength of the historical and compositional signals in phylogenetic data.{lambda} quantifies loss of historical signal, with{lambda} = 0.0 indicating evidence of a strong historical signal and{lambda} = 1.0 indicating evidence of a fully eroded historical signal.{delta} CFS quantifies compositional distance from full symmetry of a divergence matrix generated by comparing two sequences, with{delta} CFS = 0.0 indicating no evidence of evolution under dissimilar conditions and{delta} CFS > 0.0 indicating increasing evidence of lineages diverging under different conditions. The metrics are implemented in methods intended for use after multiple sequence alignment and before model selection and phylogenetic analysis. Results generated using these methods allow users of phylogenetic tools to select phylogenetic data more wisely than it previously was possible. The merits of these metrics and methods are illustrated using simulated data and multi-gene alignments obtained from 144 insect genomes.

evolutionary biology↗

Genomic adaptations to aquatic and aerial life in mayflies and the origin of wings in insects

The first winged insects underwent profound morphological and functional transformations leading to the most successful animal radiations in the history of earth. Despite this, we still have a very incomplete picture of the changes in their genomes that underlay this radiation. Mayflies (Ephemeroptera) are one of the extant sister groups of all other winged insects and therefore are at a key phylogenetic position to understand this radiation. Here, we describe the genome of the cosmopolitan mayfly Cloeon dipterum and study its expression along development and in specific organs. We discover an expansion of odorant-binding proteins, some expressed specifically in the breathing gills of aquatic nymphs, suggesting a novel sensory role for gills. In contrast, as flying adults, mayflies make use of an enlarged set of opsins and utilise these visual genes in a sexually dimorphic manner, with some opsins expressed only in males. Finally, to illuminate the origin of wings, we identify a core set of deeply conserved wing-specific genes at the root of the pterygote insects. Globally, this is the first comprehensive study of the structure and expression of the genome of a paleopteran insect and shows how its genome has kept a record of its functional adaptations.

evolutionary biology↗

Software for detecting heterogeneous evolutionary processes across aligned sequence data

Most model-based molecular phylogenetic methods assume that the sequences diverged on a tree under homogeneous conditions. If evolution occurred under these conditions, then it is unlikely that the sequences would become compositionally heterogeneous. Conversely, if the sequences are compositionally heterogeneous, then it is unlikely that they have evolved under homogeneous conditions. We present methods to detect and analyse heterogeneous evolution in aligned sequence data and to examine--visually and numerically--its effect on phylogenetic estimates. The methods are implemented in three programs, allowing users to better examine under what conditions their phylogenetic data may have evolved.

evolutionary biology↗

The genome of the blind soil-dwelling and ancestrally wingless dipluran Campodea augens, a key reference hexapod for studying the emergence of insect innovations

The dipluran two-pronged bristletail Campodea augens is a blind ancestrally wingless hexapod with the remarkable capacity to regenerate lost body appendages such as its long antennae. As sister group to Insecta (sensu stricto), Diplura are key to understanding the early evolution of hexapods and the origin and evolution of insects. Here we report the 1.2-Gbp draft genome of C. augens and results from comparative genomic analyses with other arthropods. In C. augens we uncovered the largest chemosensory gene repertoire of ionotropic receptors in the animal kingdom, a massive expansion which might compensate for the loss of vision. We found a paucity of photoreceptor genes mirroring at the genomic level the secondary loss of an ancestral external photoreceptor organ. Expansions of detoxification and carbohydrate metabolism gene families might reflect adaptations for foraging behaviour, and duplicated apoptotic genes might underlie its high regenerative potential.\n\nThe C. augens genome represents one of the key references for studying the emergence of genomic innovations in insects, the most diverse animal group, and opens up novel opportunities to study the under-explored biology of diplurans.

genomics↗

Genomic signatures accompanying the dietary shift to phytophagy in polyphagous beetles

BackgroundThe diversity and evolutionary success of beetles (Coleoptera) are proposed to be related to the diversity of plants on which they feed. Indeed the largest beetle suborder, Polyphaga, mostly includes plant-eaters among its ~315,000 species. In particular, plants defend themselves with a diversity of specialized toxic chemicals. These may impose selective pressures that drive genomic diversification and speciation in phytophagous beetles. However, evidence of changes in beetle gene repertoires driven by such interactions remains largely anecdotal and without explicit hypothesis testing.\n\nResultsTo address this, we explored the genomic consequences of beetle-plant trophic interactions by performing comparative gene family analyses across 18 species representing the two most species-rich beetle suborders. We contrasted the gene contents of species from the mostly plant-eating suborder Polyphaga with those of the mainly predatory Adephaga. We found gene repertoire evolution to be more dynamic, with significantly more adaptive lineage-specific expansions, in the more speciose Polyphaga. Testing the specific hypothesis of adaptation to plant-feeding, we identified families of enzymes putatively involved in beetle-plant interactions that underwent adaptive expansions in Polyphaga. There was especially strong support for the selection hypothesis on large gene families for glutathione S-transferase and carboxylesterase detoxification enzymes.\n\nConclusionsOur explicit modeling of the evolution of gene repertoires across 18 species identifies adaptive lineage-specific gene family expansions that accompany the dietary shift towards plants in beetles. These genomic signatures support the popular hypothesis of a key role for interactions with plant chemical defenses, and for plant-feeding in general, in driving beetle diversification.

evolutionary biology↗

A Posteriori Evaluation Of Molecular Divergence Dates Using Empirical Estimates Of Time-Heterogeneous Fossilization Rates

The application of molecular clock concepts in phylogenetics permits estimating the divergence times of clades with an incomplete fossil record. However, the reliability of this approach is disputed, because the resulting estimates are often inconsistent with different sets of fossils and other parameters (clock models and prior settings) in the analyses. Here, we present the {lambda} statistic, a likelihood approach for a posteriori evaluating the reliability of estimated divergence times. The {lambda} statistic is based on empirically derived fossilization rates and evaluates the fit of estimated divergence times to the fossil record. We tested the performance of this measure with simulated data sets. Furthermore, we applied it to the estimated divergence times of (i) Clavigeritae beetles of the family Staphylinidae and (ii) all extant insect orders. The reanalyzed beetle data supports the originally published results, but shows that several fossil calibrations used do not increase the reliability of the divergence time estimates. Analyses of estimated inter-ordinal insect divergences indicate that uniform priors with soft bounds marginally outperform log-normal priors on node ages. Furthermore, a posteriori evaluation of the original published analysis indicates that several inter-ordinal divergence estimates might be too young. The {lambda} statistic allows the comparative evaluation of any clade divergence estimate derived from different calibration approaches. Consequently, the application of different algorithms, software tools, and calibration schemes can be empirically assessed.

paleontology↗