Evolutionary adaptation is generally thought to occur through incremental mutational steps, but large mutational leaps can occur during its early stages. These are challenging to study in nature due to the difficulty of observing new genetic variants as they arise and spread, but characterizing their genomic dynamics is important for understanding factors favoring rapid adaptation. Here, we report genomic consequences of recent, adaptive song loss in a Hawaiian population of field crickets (Teleogryllus oceanicus).A discrete genetic variant, flatwing, appeared and spread approximately 15 years ago. Flatwing erases sound-producing veins on male wings. These silent flatwing males are protected from a lethal, eavesdropping parasitoid fly. We sequenced, assembled and annotated the cricket genome, produced a linkage map, and identified a flatwing quantitative trait locus covering a large region of the X chromosome. Gene expression profiling showed that flatwing is associated with extensive genome-wide effects on embryonic gene expression. We found that flatwing male crickets express feminized chemical pheromones. This male feminizing effect, on a different sexual signaling modality, is genetically associated with the flatwing genotype. Our findings suggest that the early stages of evolutionary adaptation to extreme pressures can be accompanied by greater genomic and phenotypic disruption than previously appreciated, and highlight how abrupt adaptation might involve suites of traits that arise through pleiotropy or genomic hitchhiking.

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Genomic data are transforming our understanding of biodiversity and, under the umbrella of the Earth BioGenome Project (EBP - https://www.earthbiogenome.org), many initiatives seek to generate large numbers of reference genome sequences. The distributed nature of this work makes coordination essential to ensure optimal synergy between projects and to prevent duplication of effort. While public sequence databases hold data describing completed projects, there is currently no global source of information about projects in progress or planned. In addition, the scoping and delivery of sequencing projects benefits from prior estimates of genome size and karyotype, but existing data are scattered in the literature. To address these issues, the Tree of Life programme (https://www.sanger.ac.uk/programme/tree-of-life/) has developed Genomes on a Tree (GoaT), an ElasticSearch-powered, taxon-centred database that collates observed and estimated genome-relevant metadata—including genome sizes and karyotypes—for eukaryotic species. Missing values for individual species are estimated from phylogenetic comparison. GoaT also holds declarations of actual and planned activity, from priority lists and in-progress status, to submissions to the International Nucleotide Sequence Database Collaboration (INSDC https://www.insdc.org/), across genome sequencing consortia. GoaT can be queried through a mature API (application programming interface), and we have developed a web front-end that includes data summary visualisations (see https://goat.genomehubs.org/). We are currently transitioning this service into the Tree of Life production pipeline. GoaT currently reports priority lists from the Darwin Tree of Life project (focussed on the biodiversity of Britain and Ireland). We are actively soliciting additional data concerning progress and intent from other projects so that GoaT displays a real-time summary of the state of play in reference genome sequencing, and thus facilitates collaboration and cooperation among projects. We are developing standard formats and procedures so that any project can make explicit its intent and progress. Cross referencing to other data systems such as the INSDC sequence databases, the BOLD DNA barcodes resource and Global Biodiversity Information Facility- and Open Tree of Life-related taxonomic and distribution databases will further enhance the system’s utility. We also seek to incorporate additional kinds of metadata, such as sex chromosome systems, to augment the utility of GoaT in supporting the global genome sequencing effort.

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