Stankowski Sean, Chase Madeline A, McIntosh Hanna, Streisfeld Matthew A
Institute of Ecology and Evolution, University of Oregon, Eugene, Oregon, USA.
Mol Ecol. 2023 Apr;32(8):2041-2054. doi: 10.1111/mec.16849. Epub 2023 Jan 29.
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.
理解生殖隔离的表型和遗传结构是物种形成研究的一个长期目标。在多个系统中，已经鉴定出了导致隔离表型的大效应基因座，但对于更复杂的遗传结构，这种因果关系却鲜为人知。在本研究中，我们将“自上而下”和“自下而上”的方法与种群统计学模型相结合，以综合理解猴面花杂交带的物种形成。先前的研究表明，传粉者访花行为是橙色猴面花两种不同的红花和黄花生态型之间基因流动的主要障碍。已经鉴定出了几个在分歧选择下的候选隔离性状和匿名单核苷酸多态性位点，但其基因组位置仍然未知。在这里，我们报告了种群统计学分析结果表明，这个杂交带是由二次接触形成的，但随后的基因流动受到全基因组广泛分布的障碍基因座的限制。使用一种基于地理渐变的新型基因组扫描，我们证明候选障碍基因座广泛分布于整个基因组，而不是定位到一个或几个“物种形成岛”。数量性状基因座（QTL）定位显示，大多数花部性状是高度多基因的，几乎没有证据表明QTL共定位在一起，这表明大多数性状在遗传上是独立的。最后，我们几乎没有发现QTL和候选障碍基因座重叠的证据，这表明一些基因座促成了其他形式的生殖隔离。我们的研究结果突出了理解生殖隔离遗传结构的挑战，并揭示出除传粉者隔离之外的基因流动障碍可能在这个系统中发挥重要作用。
