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 study an adaptive radiation of Cyprinodon pupfishes in Laguna Chichancanab, Mexico, compared to previous research on an independent radiation of San Salvador Island (SSI) pupfishes in the Bahamas, to assess the repeatability of their 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 in SSI, we found minimal evidence of adaptive introgression in Chichancanab, likely due to the higher geographical isolation of this inland lake. Instead, de novo mutations provided a substantial source of adaptive variation (30.6%) for the endemic zooplanktivore, nearly 10 times higher than the scale-eater in 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. Unique to Chichancanab, adaptive variants near opsin and spermatogenesis genes are consistent with our findings of greater visual acuity and differences in sperm morphology, respectively, within the zoooplanktivore. Our study suggests that de novo mutations may contribute more to rapid adaptive radiations than previously appreciated, particularly in isolated environments.