Unlike hexapods and vertebrates, in chelicerates, knowledge of the specific molecules involved in chemoreception comes exclusively from the comparative analysis of genome sequences. Indeed, the genomes of mites, ticks and spiders contain several genes encoding homologs of some insect membrane receptors and small soluble chemosensory proteins. Here, we conducted for the first time a comprehensive comparative RNA-Seq analysis across different body structures of a chelicerate: the nocturnal wandering hunter spider Dysdera silvatica Schmidt 1981. Specifically, we obtained the complete transcriptome of this species as well as the specific expression profile in the first pair of legs and the palps, which are thought to be the specific olfactory appendages in spiders, and in the remaining legs, which also have hairs that have been morphologically identified as chemosensory. We identified several ionotropic (Ir) and gustatory (Gr) receptor family members exclusively or differentially expressed across transcriptomes, some exhibiting a distinctive pattern in the putative olfactory appendages. Furthermore, these IRs were the only known olfactory receptors identified in such structures. These results, integrated with an extensive phylogenetic analysis across arthropods, uncover a specialization of the chemosensory gene repertoire across the body of D. silvatica and suggest that some IRs likely mediate olfactory signaling in chelicerates. Noticeably, we detected the expression of a gene family distantly related to insect odorant-binding proteins (OBPs), suggesting that this gene family is more ancient than previously believed, as well as the expression of an uncharacterized gene family encoding small globular secreted proteins, which appears to be a good chemosensory gene family candidate.

Chemoreception is a widespread biological function that is essential for the survival, reproduction, and social communication of animals. Though the molecular mechanisms underlying chemoreception are relatively well known in insects, they are poorly studied in the other major arthropod lineages. Current availability of a number of chelicerate genomes constitutes a great opportunity to better characterize gene families involved in this important function in a lineage that emerged and colonized land independently of insects. At the same time, that offers new opportunities and challenges for the study of this interesting animal branch in many translational research areas. Here, we have performed a comprehensive comparative genomics study that explicitly considers the high fragmentation of available draft genomes and that for the first time included complete genome data that cover most of the chelicerate diversity. Our exhaustive searches exposed thousands of previously uncharacterized chemosensory sequences, most of them encoding members of the gustatory and ionotropic receptor families. The phylogenetic and gene turnover analyses of these sequences indicated that the whole-genome duplication events proposed for this subphylum would not explain the differences in the number of chemoreceptors observed across species. A constant and prolonged gene birth and death process, altered by episodic bursts of gene duplication yielding lineage-specific expansions, has contributed significantly to the extant chemosensory diversity in this group of animals. This study also provides valuable insights into the origin and functional diversification of other relevant chemosensory gene families different from receptors, such as odorant-binding proteins and other related molecules.

The evolution of winged insects revolutionized terrestrial ecosystems and led to the largest animal radiation on Earth. However, we still have an incomplete picture of the genomic changes that underlay this diversification. Mayflies, as one of the sister groups of all other winged insects, are key to understanding this radiation. Here, we describe the genome of the mayfly Cloeon dipterum and its gene expression throughout its aquatic and aerial life cycle and specific organs. We discover an expansion of odorant-binding-protein genes, some expressed specifically in breathing gills of aquatic nymphs, suggesting a novel sensory role for this organ. In contrast, flying adults use an enlarged opsin set in a sexually dimorphic manner, with some expressed only in males. Finally, we identify a set of wing-associated genes deeply conserved in the pterygote insects and find transcriptomic similarities between gills and wings, suggesting a common genetic program. Globally, this comprehensive genomic and transcriptomic study uncovers the genetic basis of key evolutionary adaptations in mayflies and winged insects.

Gene annotation is a critical bottleneck in genomic research, especially for the comprehensive study of very large gene families in the genomes of nonmodel organisms. Despite the recent progress in automatic methods, state‐of‐the‐art tools used for this task often produce inaccurate annotations, such as fused, chimeric, partial or even completely absent gene models for many family copies, errors that require considerable extra efforts to be corrected. Here we present bitacora, a bioinformatics solution that integrates popular sequence similarity‐based search tools and Perl scripts to facilitate both the curation of these inaccurate annotations and the identification of previously undetected gene family copies directly in genomic DNA sequences. We tested the performance of bitacora in annotating the members of two chemosensory gene families with different repertoire size in seven available genome sequences, and compared its performance with that of augustus‐ppx, a tool also designed to improve automatic annotations using a sequence similarity‐based approach. Despite the relatively high fragmentation of some of these drafts, bitacora was able to improve the annotation of many members of these families and detected thousands of new chemoreceptors encoded in genome sequences. The program creates general feature format (GFF) files, with both curated and newly identified gene models, and FASTA files with the predicted proteins. These outputs can be easily integrated in genomic annotation editors, greatly facilitating subsequent manual annotation and downstream evolutionary analyses.

The coexistence of multiple eco‐phenotypes in independently assembled communities makes island adaptive radiations the ideal framework to test convergence and parallelism in evolution. In the radiation of the spider genus Dysdera in the Canary Islands, species diversification occurs concomitant with repeated events of trophic specialization. These dietary shifts, to feed primarily on woodlice, are accompanied by modifications in morphology (mostly in the mouthparts), behaviour and nutritional physiology. To gain insight into the molecular basis of this adaptive radiation, we performed a comprehensive comparative transcriptome analysis of five Canary Island Dysdera endemics representing two evolutionary and geographically independent events of dietary specialization. After controlling for the potential confounding effects of hemiplasy, our differential gene expression and selective constraint analyses identified a number of genetic changes that could be associated with the repeated adaptations to specialized diet of woodlice, including some related to heavy metal detoxification and homeostasis, the metabolism of some important nutrients and venom toxins. Our results shed light on the genomic basis of an extraordinary case of dietary shift convergence associated with species diversification. We uncovered putative molecular substrates of convergent evolutionary changes at different hierarchical levels, including specific genes, genes with equivalent functions and even particular amino acid positions. This study improves our knowledge of rapid adaptive radiations and provides new insights into the predictability of evolution.