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Structural elements are widespread across genomes, but their complexity and role in repeatedly driving local adaptation remain unclear. In this work, we use phased genome assemblies to show that adaptive divergence in cryptic color pattern in a stick insect is repeatedly underlain by structural variation, but not a simple chromosomal inversion. We found that color pattern in populations of stick insects on two mountains is associated with translocations that have also been inverted. These translocations differ in size and origin on each mountain, but they overlap partially and involve some of the same gene regions. Moreover, this structural variation is subject to divergent selection and arose without introgression between species. Our results show how the origin of structural variation provides a mechanism for repeated bouts of adaptation. 

The extent to which evolution is repeatable remains debated. Here, we study changes over time in the frequency of cryptic color-pattern morphs in 10 replicate long-term field studies of a stick insect, each spanning at least a decade (across 30 years of total data). We find predictable “up-and-down” fluctuations in stripe frequency in all populations, representing repeatable evolutionary dynamics based on standing genetic variation. A field experiment demonstrates that these fluctuations involve negative frequency-dependent natural selection (NFDS). These fluctuations rely on demographic and selective variability that pushes populations away from equilibrium, such that they can reliably move back toward it via NFDS. Last, we show that the origin of new cryptic forms is associated with multiple structural genomic variants such that which mutations arise affects evolution at larger temporal scales. Thus, evolution from existing variation is predictable and repeatable, but mutation adds complexity even for traits evolving deterministically under natural selection.