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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. 

There is increasing evidence that genetic evolution can occur rapidly enough to affect the ecological dynamics of populations and communities ( 1 – 3 ). To better predict the future of ecosystems, it is necessary to understand how evolutionary changes within species influence and interact with ecological changes through processes known as “eco-evolutionary dynamics” ( 4 ). On page 70 of this issue, Barbour et al. ( 5 ) demonstrate that a gene affecting a plant’s resistance to herbivory also influences the persistence of the food web through the gene’s effect on plant growth (see the figure). Subsequent studies of natural selection in the wild can help explain how variations of such “keystone genes” can be maintained ( 6 , 7 ). The maintenance of genetic variation in keystone genes is required for eco-evolutionary dynamics to be perpetual rather than transient. 

The types of mutations affecting adaptation in the wild are only beginning to be understood. In particular, whether structural changes shape adaptation by suppressing recombination or by creating new mutations is unresolved. Here, we show that multiple linked but recombining loci underlie cryptic color morphs of Timema chumash stick insects. In a related species, these loci are found in a region of suppressed recombination, forming a supergene. However, in seven species of Timema , we found that a megabase-size “supermutation” has deleted color loci in green morphs. Moreover, we found that balancing selection likely contributes more to maintaining this mutation than does introgression. Our results show how suppressed recombination and large-scale mutation can help to package gene complexes into discrete units of diversity such as morphs, ecotypes, or species.