Integrating top-down and bottom-up approaches to understand the genetic architecture of speciation across a monkeyflower hybrid zone

Abstract

Understanding the phenotypic and genetic architecture of reproductive isolation is a longstanding goal of speciation research. In many systems, candidate barrier traits and loci have been identified, but causal connections between them are rarely made. In this study, we combine ‘top-down’ and ‘bottom-up’ approaches with demographic modeling toward an integrated understanding of speciation across a monkeyflower hybrid zone. Previous work in this system suggests that pollinator-mediated reproductive isolation is a primary barrier to gene flow between two divergent red- and yellow-flowered ecotypes of Mimulus aurantiacus. Several candidate floral traits contributing to pollinator isolation have been identified, including a difference in flower color, which is caused primarily by a single large-effect locus (MaMyb2). Other anonymous SNP loci, potentially contributing to pollinator isolation, also have been identified, but their causal relationships remain untested. Here, we performed demographic analyses, which indicate that this hybrid zone formed by secondary contact, but that subsequent gene flow was restricted in a large fraction of the genome by barrier loci. Using a cline-based genome scan (our bottom-up approach), we demonstrate that candidate barrier loci are broadly distributed across the genome, rather than mapping to one or a few ‘islands of speciation.’ A QTL analysis (our top-down approach) revealed most floral traits are highly polygenic, with little evidence that QTL co-localize, indicating that most traits are largely genetically independent. Finally, we find little convincing evidence for the overlap of QTL and candidate barrier loci, suggesting that some loci contribute to other forms of reproductive isolation. Our findings highlight the challenges of understanding the genetic architecture of reproductive isolation and reveal that barriers to gene flow aside from pollinator isolation may play an important role in this system.