We get by with a little help from our friends: diversity begets diversity through shared adaptive genetic variation

Abstract

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 ‘wide-mouth’ intermediate scale-eating ecomorph in a sympatric 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 C. sp. ‘wide-mouth’ scale-eating niche aided in the rapid divergence of the more specialized scale-eater C. desquamator. Therefore, selection for shared adaptive variants should 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 desquamator 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 molluscivore 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. Author Summary Adaptive radiations present a paradox to our understanding of the mechanisms that drive speciation. The hallmark of adaptive radiation is a rapid, sustained burst of ecological, phenotypic, and species diversity yet many theoretical models predict that diversification should slow down with each event. Alternatively, radiations could be self-propagating and the diversity generated within the first stages of radiation could beget further diversity. The microevolutionary processes underlying this hypothesis are poorly understood. We propose that the exchange of adaptive alleles from one population could help other populations colonize new fitness peaks and promote further diversification across the fitness landscape. Here we explore the role of shared adaptive alleles in a recent radiation of trophic specialist pupfishes and characterize a cryptic new scale-eating species (C. sp. ‘wide-mouth’) through morphological, dietary, and genomic analyses. We discovered shared selective sweeps among all three specialists in this radiation despite their divergent morphologies and ecologies. We also found that adaptive introgression from the more specialized scale-eater C. desquamator may have provided access to a similar niche in the recently discovered intermediate scale-eater. Our findings of shared adaptive alleles and selective sweeps across multiple specialists within a radiation provide support for the hypothesis that diversity begets diversity and insight into the underlying microevolutionary process.