Quantity, Not Quality: Rapid Adaptation in a Polygenic Trait Proceeded Exclusively through Expression Differentiation

A trait's genomic architecture can affect the rate and mechanism of adaptation, and although many ecologically-important traits are polygenic, most studies connecting genotype, phenotype, and fitness in natural populations have focused on traits with relatively simple genetic bases. To understand the genetic basis of polygenic adaptation, we must integrate genomics, phenotypic data, ecology, and fitness effects for a genetically tractable, polygenic trait; snake venoms provide such a system for studying polygenic adaptation because of their genetic tractability and vital ecological role in feeding and defense. We used a venom transcriptome-proteome map, quantitative proteomics, genomics, and fitness assays in sympatric prey to construct a genotype-phenotype-fitness map for the venoms of an island-mainland pair of rattlesnake populations. Reciprocal fitness experiments demonstrated that each population was locally adapted to sympatric prey. We identified significant expression differentiation with little to no coding-sequence variation across populations, demonstrating that expression differentiation was exclusively the genetic basis of polygenic adaptation. Previous research on the genetics of adaptation, however, has largely been biased toward investigating protein-coding regions because of the complexity of gene regulation. Our results showed that biases at the molecular level can be in the opposite direction, highlighting the need for more systematic comparisons of different molecular mechanisms underlying rapid, adaptive evolution in polygenic traits.