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Further information about methodology and results

Further methods and figures

Further details of the methods included in the main document, including supplementary figures and tables

Funding:TJH was supported by a PhD studentship from the University of St Andrews School of Biology. The study received funding from the UK Natural Environment Research Council to NWB and JGR (NE/T0006191/1) and NWB (NE/L011255/1, NE/I027800/1). Recent theory has suggested that dosage compensation mediates sexual antagonism over X-linked genes. This process relies on the assumption that dosage compensation scales phenotypic effects between the sexes, which is largely untested. We evaluated this by quantifying transcriptome variation associated with a recently arisen, male-beneficial, X-linked mutation across tissues of the field cricket Teleogryllus oceanicus, and testing the relationship between the completeness of dosage compensation and female phenotypic effects at the level of gene expression. Dosage compensation in T. oceanicus was variable across tissues but usually incomplete, such that relative expression of X-linked genes was typically greater in females. Supporting the assumption that dosage compensation scales phenotypic effects between the sexes, we found tissues with incomplete dosage compensation tended to show female-skewed effects of the X-linked allele. In gonads, where expression of X-linked genes was most strongly female-biased, ovaries-limited genes were much more likely to be X-linked than were testes-limited genes, supporting the view that incomplete dosage compensation favours feminization of the X. Our results support the expectation that sex chromosome dosage compensation scales phenotypic effects of X-linked genes between sexes, substantiating a key assumption underlying the theoretical role of dosage compensation in determining the dynamics of sexual antagonism on the X. Postprint

The Natural Environment Research Council provided funding to N.W.B. (NE/G014906/1, NE/L011255/1) and to N.W.B. and M.G.R. (NE/1027800/1). Sequencing was provided by Edinburgh Genomics and the Centre for Genomic Research (University of Liverpool). Bioinformatics resources at St Andrews were funded by the Wellcome Trust (105621/Z/14/Z). Support from the China Scholarship Council (201703780018) to X.Z. is gratefully acknowledged. The Biotechnology and Biological Sciences Research Council provided support to M.B. for development of ChirpBase (BB/K020161/1). 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. Publisher PDF