Parallel and non-parallel features of adaptive radiation in Yucatán pupfishes

Understanding the extent of parallelism across adaptive radiations remains a central problem in evolutionary biology. We used whole-genome resequencing of 123 individuals to compare an adaptive radiation of Cyprinodon pupfishes in Laguna Chichancanab, Mexico, to an independent radiation of San Salvador Island (SSI) pupfishes in the Bahamas, and assess the repeatability of adaptive genetic architecture, sources of adaptive variation, and stages of selection. Despite rapid craniofacial divergence of trophic specialists within 8-15 kya, only two candidate genes (3.6%) were shared between Caribbean radiations. Although adaptive introgression played a major role on SSI, we found minimal evidence of adaptive introgression in Chichancanab, likely due to geographic isolation of this inland lake. Instead, de novo mutations provided a substantial source of adaptive variation (30.6%) for the endemic zooplanktivore, 15.3 times higher than the endemic scale-eater on SSI. We found strong evidence that selection occurred in stages, first on regulatory and standing genetic variation, then on de novo and nonsynonymous mutations, parallel to SSI. We then verified that adaptive variants near vision-development and spermatogenesis genes, uniquely within Chichancanab, are consistent with greater visual acuity and divergent sperm morphology in the zoooplanktivore. Consistent with extensive adaptive de novo mutations in WNT10A and rapid diversification of tooth size in the zooplanktivore, we found that experimental inhibition of this pathway in generalists results in narrower teeth. We conclude that de novo mutations, not introgression, can drive rapid adaptive radiations in isolated environments.