Regulatory divergence in vgll3 underlies variation in age at maturity in male Atlantic salmon

The optimal phenotypes to survive and reproduce in given evolutionary settings are often in conflict, which manifest as trade-offs in life history traits. Genome-wide association studies have been successful in uncovering genome regions controlling for life history trade-offs in a range of species 1–8 . However, lack of functional studies of the discovered genotype-phenotype associations restrains our understanding how alternative life history traits evolved and are mediated at the molecular level. Here we establish a molecular mechanism by which allele-specific expression differences of the transcription co-factor vgll3 mediate variation in age at maturity in male Atlantic salmon ( Salmo salar ). By way of a common-garden experiment and temporal sampling of vgll3 expression, we show that vgll3 genotype and expression control male puberty timing in one-year old salmon. Vgll3 expression was high in immature testicular tissue and males entering puberty reduced their vgll3 expression by 66% compared to immature males. Testicular expression of the early maturation associated allele in immature males was constitutively lower compared to the late maturation allele, shifting the liability of early allele carriers towards earlier maturation. These results reveal how gene regulatory differences can be a central mechanism for the evolution of life history variation.