Yosemite Toad (Anaxyrus canorus) transcriptome reveals interplay between speciation genes and adaptive introgression

Genomes are 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 diverge,
secondary contact zones between them can act as an interface, and
selectively filter through advantageous alleles of hybrid origin. Such
introgression is another important adaptive process, one that allows
beneficial mosaics of recombinant DNA (“rivers”) to flow from one species
into another. Although genomic islands of divergence appear to be
associated with reproductive isolation, and genomic rivers form by
adaptive introgression, it is unknown whether islands and rivers tend to
be the same or different loci. We examined three replicate secondary
contact zones for the Yosemite toad (Anaxyrus canorus) using 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 loci are first islands, and
later are predictably converted into rivers. However, 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 potentially involved in climate change adaptation, that is
island-like for all three contact zones but also appears to be
introgressing (as a river) across one zone. Taken together, our results
suggest that adaptive divergence and introgression may be more
complementary forces than currently appreciated.