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 long‐standing goal of speciation research. In several systems, large‐effect loci contributing to barrier phenotypes have been characterized, but such causal connections are rarely known for more complex genetic architectures. In this study, we combine “top‐down” and “bottom‐up” approaches with demographic modelling toward an integrated understanding of speciation across a monkeyflower hybrid zone. Previous work suggests that pollinator visitation acts as a primary barrier to gene flow between two divergent red‐ and yellow‐flowered ecotypes of Mimulus aurantiacus. Several candidate isolating traits and anonymous single nucleotide polymorphism loci under divergent selection have been identified, but their genomic positions remain unknown. Here, we report findings from demographic analyses that indicate this hybrid zone formed by secondary contact, but that subsequent gene flow was restricted by widespread barrier loci across the genome. Using a novel, geographic cline‐based genome scan, we demonstrate that candidate barrier loci are broadly distributed across the genome, rather than mapping to one or a few “islands of speciation.” Quantitative trait locus (QTL) mapping reveals that most floral traits are highly polygenic, with little evidence that QTL colocalize, indicating that most traits are genetically independent. Finally, we find little evidence that QTL and candidate barrier loci overlap, 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 other than pollinator isolation may play an important role in this system.

The genetic architecture of polygenic local adaptation and its role in shaping barriers to gene flow

“…5). Recent findings such as those of Stankowski et al . (2023) emphasize that readily discovered large-effect loci which bear a clear relationship to locally adaptive traits may often be associated with a polygenic background whose causal connection with local adaptation is less obvious.…”

“…While local adaptation may be driven by a few conspicuous loci (e.g. adaptive melanism in peppermoths (van't Hof et al 2016) or pocket mice (Nachman et al 2003)), it is believed to typically be polygenic, involving alleles of different effect at many loci across the genome (Pritchard and Di Rienzo 2010;Le Corre and Kremer 2012;Westram et al 2018;Barghi et al 2020;Bomblies and Peichel 2022;Stankowski et al 2023). When local adaptation is polygenic, migration from a population adapted to different environmental conditions will generate linkage disequilibria (LD) among selected loci, and the rate at which each individual invading locally deleterious allele is eliminated will be affected by such associations, a phenomenon often referred to as a 'coupling' effect (Barton 1983;Kruuk et al 1999;Feder et al 2012;Yeaman 2015;Sachdeva 2022).…”

Ancient hybridization leads to the repeated evolution of red flowers across a monkeyflower radiation

“…Multiple lines of evidence support the presence of geographically widespread and recent positive selection in the red ecotype in San Diego. Specifically, despite ongoing gene flow between the ecotypes, there is a steep geographic cline in both allele frequency and ancestry at this locus (Streisfeld et al 2013;Stankowski et al 2023), and this locus shows a unique pattern of divergence relative to the rest of the genome (Stankowski et al 2017;2019). However, it is unclear whether the other red-flowered samples also show evidence of positive selection following introgression.…”

How the switch to hummingbird pollination has greatly contributed to our understanding of evolutionary processes

“…For example, in M. aurantiacus, hummingbird-vs hawkmoth-adapted ecotypes hybridize where ranges overlap. Although flower color differences between ecotypes involve a major-effect locus (Streisfeld et al, 2013), divergence in other floral traits involves many loci of small effect that are scattered throughout the genome (Stankowski et al, 2023). Genomic intervals that overlap floral QTLs do not exhibit elevated differentiation between ecotypes, suggesting these regions do not strongly resist gene flow relative to the genome-wide average (Stankowski et al, 2023).…”

“…Although flower color differences between ecotypes involve a major-effect locus (Streisfeld et al, 2013), divergence in other floral traits involves many loci of small effect that are scattered throughout the genome (Stankowski et al, 2023). Genomic intervals that overlap floral QTLs do not exhibit elevated differentiation between ecotypes, suggesting these regions do not strongly resist gene flow relative to the genome-wide average (Stankowski et al, 2023). Louisiana Irises show similar patterns: Admixture mapping in natural hybrid zones formed by the bee-adapted Iris hexagona and hummingbird-adapted I. fulva revealed most floral traits have a polygenic architecture of smalleffect loci distributed throughout the genome that, again, are not particularly resistant to gene flow compared with genome-wide background patterns (Sung et al, 2018).…”