A few essential genetic loci distinguish Penstemon species with flowers adapted to pollination by bees or hummingbirds

In the formation of species, adaptation by natural selection generates distinct combinations of traits that function well together. The maintenance of adaptive trait combinations in the face of gene flow depends on the strength and nature of selection acting on the underlying genetic loci. Floral pollination syndromes exemplify the evolution of trait combinations adaptive for particular pollinators. The North American wildflower genus Penstemon displays remarkable floral syndrome convergence, with at least 20 separate lineages that have evolved from ancestral bee pollination syndrome (wide blue-purple flowers that present a landing platform for bees and small amounts of nectar) to hummingbird pollination syndrome (bright red narrowly tubular flowers offering copious nectar). Related taxa that differ in floral syndrome offer an attractive opportunity to examine the genomic basis of complex trait divergence. In this study, we characterized genomic divergence among 229 individuals from a Penstemon species complex that includes both bee and hummingbird floral syndromes. Field plants are easily classified into species based on phenotypic differences and hybrids displaying intermediate floral syndromes are rare. Despite unambiguous phenotypic differences, genomewide differentiation between species is minimal. Hummingbird-adapted populations are more genetically similar to nearby bee-adapted populations than to geographically distant hummingbird-adapted populations, in terms of genomewide dXY. However, a small number of genetic loci are strongly differentiated between species. These ~ 20 "species-diagnostic loci", which appear to have nearly fixed differences between pollination syndromes, are sprinkled throughout the genome in high recombination regions. Several map closely to previously established floral trait QTLs. The striking difference between the diagnostic loci and the genome as whole suggests strong selection to maintain distinct combinations of traits, but with sufficient gene flow to homogenize the genomic background. A surprisingly small number of alleles confer phenotypic differences that form the basis of species identity in this species complex.

在物种形成过程中，自然选择介导的适应性演化会产生功能协同的差异化性状组合。在存在基因流的情况下，适应性性状组合的维持取决于作用于其背后遗传位点的选择强度与选择性质。花部传粉综合征（floral pollination syndrome）是针对特定传粉者演化出适配性状组合的典型范例。北美野生花卉类群钓钟柳属（Penstemon）展现出极为显著的花部传粉综合征趋同演化特征，至少存在20个独立演化支系，从祖先类群的蜂类传粉综合征（花冠宽阔呈蓝紫色，可为蜂类提供降落平台且花蜜含量较少）演化为蜂鸟传粉综合征（花冠窄管状、色泽鲜红且花蜜储量丰富）。花部传粉综合征存在差异的近缘类群，为解析复杂性状分化的基因组基础提供了极佳的研究契机。本研究针对同时涵盖蜂类与蜂鸟传粉综合征的钓钟柳属物种复合群，对来自该类群的229个个体开展了基因组分化特征分析。野外植株可依据表型差异轻松归类至相应物种，且表现出中间型花部综合征的杂交个体极为罕见。尽管两类群间表型差异明确，但全基因组水平的物种分化程度却极低。以全基因组核苷酸分歧度（dXY）为指标来看，适应蜂鸟的种群与邻近的蜂类适应种群的遗传相似度，高于其与地理距离更远的蜂鸟适应种群的遗传相似度。但仍有少量遗传位点在两类群间呈现显著分化。这些约20个‘物种诊断位点’在传粉综合征类群间几乎存在固定差异，且广泛分布于基因组的高重组区域中。其中多个位点与此前已报道的花部性状数量性状基因座（quantitative trait locus, QTL）紧密连锁。诊断位点与全基因组整体水平的分化差异如此显著，表明存在强烈的选择压力以维持差异化的性状组合，但同时也存在足够的基因流以均质化基因组背景。本物种复合群中，仅需极少量等位基因即可介导表型差异，而这些差异正是物种界定的核心依据。