Abstract
—What are the processes that shape patterns of genome-wide variation between emerging species? This question is central to our understanding of the origins of biodiversity and the fundamental principles governing molecular evolution. It is becoming clear that indirect selection on linked neutral variation (hereafter ‘linked selection’) plays a pervasive role in shaping heterogeneous patterns of genome-wide diversity and differentiation within and between species, but we do not know how these signatures of linked selection evolve over time. To fill this critical knowledge gap, we construct the first chromosome-level genome assembly for the bush monkeyflower, and use it to show that linked selection has been a primary architect of heterogeneous patterns of lineage sorting, differentiation, and nucleotide diversity across a recent radiation. By taking advantage of the range of divergence times between the different pairs of monkeyflower taxa, we also show how the signatures of linked selection evolve as populations diverge: linked selection occurring within lineages acts to conserve an ancestral pattern of diversity after a population split, while its joint action in separate lineages causes a common differentiation landscape to rapidly emerge between them. Together, our study demonstrates how pervasive linked selection shapes patterns of genome-wide variation within and between taxa, and provides critical insight into how its singiature evolves during the first 1.5 million years of divergence.
Significance What are the processes that shape patterns of genome-wide variation between emerging species? Because nucleotides are linked together on chromosomes, even neutral variants are impacted by selection on mutations that arise at neighboring sites. We show that this phenomenon, referred to as linked selection, was important in causing common patterns of differentiation to evolve between taxa during a radiation of monkeyflowers. This signature begins to emerge shortly after divergence begins, but it takes 1.5 million years to become pronounced. This result fills a critical gap in our knowledge about how genomes evolve, and it shows how linked selection shapes patterns of differentiation soon after a population split, which is critical to our understanding of divergence and speciation.