Epigenetic changes associated with reproductive investment and life-history trade-offs in lekking male black grouse (Lyrurus tetrix)

Rebecca Shuhua Chen , Carl D. Soulsbury, Joseph I. Hoffman, Kees van Oers

Life-history trade-offs are a central concept in evolutionary biology, yet their underlying molecular mechanisms are not yet fully understood. Whilst much research has focused on genetic variation, epigenetic mechanisms, which regulate gene regulation, may be equally important. To investigate this, we collected blood samples from 50 male black grouse (Lyrurus tetrix) before and after the breeding (lekking) period and quantified genome-wide DNA methylation changes using reduced representation bisulphite sequencing. We identified 1,026 CpG sites that changed significantly in methylation across the breeding period, many residing within genes involved in the regulation of RNA biosynthesis. We tested whether these DNA methylation changes were associated with reproductive investment and future fitness-relevant traits: survival and the expression of post-breeding sexual ornaments, which reflect body condition after the strenuous lekking period. Dozens of CpG sites showed significant associations, often clustering within the same genes, suggesting that epigenetic changes associated with reproduction and survival are localized rather than widespread. Moreover, changes at three CpG sites exhibited opposite relationships between current reproductive investment and future fitness-relevant traits, suggesting that epigenetic mechanisms might contribute to shaping life-history trade-offs. Our study demonstrates that DNA methylation changes are associated with the expression of costly reproductive traits, highlighting the importance of epigenetic mechanisms in shaping life-history traits and fitness.