Blind genomic tree scans identify loci underlying adaptive peaks in Antirrhinum

Abstract

A key question in evolutionary biology is how barriers to gene flow operate and arise between populations, leading to speciation. Barriers are typically identified by comparing populations distinguished by phenotype, geographical location and/or environment. However, such prior classifications may bias recovery towards features obvious to the human eye, influencing mechanistic interpretations. Here we develop a method blind to prior classifications. We apply it to 18 Antirrhinum populations occupying habitats from coastal to alpine. By scanning the genome for regions with deeply rooted similar trees, we identify a single multi-locus partition, comprising less than 0.5% of the genome. It derives from eight genes, three newly identified here, which interact to generate complementary pollinator guides, likely corresponding to two adaptive peaks in a fitness landscape. Hybrid genotypes fall in a fitness valley, allowing the partition to be maintained through hybrid incompatibility and creating steep clines in allele frequency at a hybrid zone. Another partition derives from a single locus linked to a gene controlling plant height. The locus exhibits a shallow cline in allele frequency across an eco-geographic barrier and may be eco-adaptive. Our results suggest that two ancestral subspecies underwent extensive gene flow except at a few barrier loci, showing how both hybrid incompatibility and eco-adaptation can operate to maintain diversity.