Diversity begets diversity through shared adaptive genetic variation: discovery of a cryptic wide-mouthed scale-eater

Summary Adaptive radiations involve astounding bursts of phenotypic, ecological, and species diversity. However, the microevolutionary processes that underlie the origins of these bursts are still poorly understood. We report the discovery of a cryptic intermediate ‘wide-mouth’ scale-eating ecomorph in a recent radiation of Cyprinodon pupfishes which provides crucial information about the evolutionary and ecological transition from a widespread algae-eating generalist to a novel microendemic scale-eating specialist. We first show that this ecomorph occurs in sympatry with generalist C. variegatus and scale-eating specialist C. desquamator across several hypersaline lakes on San Salvador Island, Bahamas, but is genetically differentiated, morphologically distinct when reared in a common garden, and sometimes consumes scales. We then compared the timing of selective sweeps on shared and unique adaptive variants in both scale-eating species to characterize the evolutionary path to scale-eating. We predicted that adaptation to the intermediate ‘wide-mouth’ scale-eating niche aided in the rapid divergence of the more specialized scale-eater C. desquamator. Therefore, selection for shared adaptive variants would occur first in ‘wide-mouth’. Contrary to our prediction, four of the six sets of shared adaptive alleles in both scale-eating species swept significantly earlier in C. desquamator. Adaptive introgression from the specialist into the ‘wide-mouth’ ancestor may have resulted in parallel evolution of their dietary niche. Conversely, no adaptive alleles for scale-eating were reused in a third sympatric specialist C. brontotheriodes, despite sharing 9% of hard selective sweeps. Our work provides a microevolutionary framework for investigating how ‘diversity begets diversity’ during adaptive radiation.