Genomic Geography: Islands and Rivers of Divergence for Yosemite Toad (Anaxyrus canorus) Contact Zones

Genomes are highly heterogeneous during the early stages of speciation, with small “islands” of DNA appearing to reflect strong adaptive differences, surrounded by vast seas of relative homogeneity. As species begin to diverge, secondary contact zones between them can act as the interface between their diverging genomes, and selectively filter through advantageous hybrid alleles. Such introgression is another important adaptive process, one that allows adaptive mosaics of recombinant DNA to flow like “rivers” from one species into the other. Although genomic islands appear to be associated with reproductive isolation, and genomic rivers form by a different process (adaptive introgression), it is unknown whether islands and rivers are actually different loci. One possibility is that islands and rivers are predictably different loci. This may happen if islands typically include “speciation genes” that evolve by the same mutations, and recombining these mutations lowers hybrid fitness, leading to reproductive isolation. Another possibility is that islands are simply small-effect, polygenic adaptations. In this scenario, numerous genes have the potential to become islands, making the genomic location of islands unpredictable. However, the extreme allele frequency differences at these island loci could fuel more extreme recombinant traits, thus turning small-effect island adaptations into more potent river adaptations. Thus, hybrid advantage from adaptive recombination may supersede any hybrid incompatibility, and predictably convert some islands into rivers. We used three replicate secondary contact zones for the Yosemite toad (Anaxyrus canorus), two genomic datasets, and a morphometric dataset to answer the questions: (1) How predictably different are islands and rivers, both in terms of genomic location and gene function; (2) Are the adaptive genetic trait loci underlying tadpole growth and development reliably islands, rivers, or neither? We found that island and river loci have significant overlap within a contact zone, suggesting that some islands are predictably converted into rivers. However, our gene ontology enrichment analysis showed strong overlap in gene function unique to all island loci, suggesting predictability in overall gene pathways for islands. GWAS outliers for tadpole development included LPIN3, a lipid metabolism gene that is nearly an island for all three contact zones, but also appears to be introgressing (as a river) across one zone. Taken together, our results suggest that a more nuanced view of islands and rivers is needed, where some islands may predictably contribute to reproductive isolation, but others play a vital role in the generation of recombinant adaptation.