The geographic structure of chloroplast capture in a hybrid zone

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Abstract
The frequency of hybridization differs strongly across different taxa and areas of Earth, yet the environmental drivers of this variation remain poorly understood. Areas strongly influenced by Pleistocene glaciation have long been hypothesized to be rich in hybrid taxa through forcing previously allopatric species into contact and interrupting ecological barriers. Here, we revisit naturally occurring Heuchera americana × H. richardsonii in North America using deep population level sampling of nuclear and plastid genomes to re-evaluate the long-standing hypothesis that Pleistocene climate dynamics promoted hybridization in this system. An extensive population-level sampling scheme involving nuclear and plastid genetic data (729 individuals across 455 populations) reveals a more complex hybridization history than implied by previous representative phylogenetic sampling. Our analyses identify multiple independent chloroplast capture events since diversification within this complex, rather than a previously hypothesized single ancestral event. Strong geographic structure at higher-level plastid clades but little structure within subclades, together with the rarity of ancestral plastid genomes, suggests a unidirectional inheritance of the introgressed plastid genome rather than a simple geographic distribution of plastid haplotypes. Ancestral niche projections indicate that Pleistocene glacial maxima created a shared narrow eastern refugium east of the Mississippi River, enabling localized hybridization, while western refugia were larger and taxa probably allopatric. This contrast led to an east-west gradient in cytonuclear discord. Our results corroborate and refine a 90-year-old hypothesis of climate-mediated hybridization by demonstrating that historical gene flow was spatially restricted but hybrid genotypes now command a larger geographic area. Our study highlights the importance of deep population-level sampling for accurately reconstructing hybridization histories and underscores the catalytic role of climatic instability in general as a driver of hybridization in Heuchera , and likely many other taxa across the tree of life.

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