History and environment shape population genetic and phytochemical variation across three western Juniperus species and their hybrids

Hybridization has been an important process in the evolutionary history of many plant species that has potential for extended ecological consequences through its effects on phenotype. Junipers (Juniperus) are foundational tree species in many semi-arid landscapes of the western United States, and hybridize frequently. Juniperus grandis, J. occidentalis, and J. osteosperma are known to hybridize in a complex zone of secondary contact in western Nevada, permitting investigation into the geographic and environmental predictors of hybridization and its phenotypic consequences. Here, we generated population genomic data (9,125 SNPs; 326 individuals; 25 populations) to quantify patterns of genetic variation across populations and species and to characterize ancestry variation in hybrids and its phytochemical consequences. Our analyses indicated that the parental species represent well-differentiated, monophyletic lineages which are phenotypically and ecologically distinct. As is common in other groups of conifers, we detected little evidence for genetic differentiation among populations within each species. Hybrids occupied environmental conditions intermediate of the parental species, generally exhibited ancestry from all three parental species, and were largely F1 and advanced generation backcrosses. We used gas chromatography mass spectrometry (GC-MS) to characterize terpenoid variation across parental species and hybrids to better understand how underlying environmental and ancestry variation shape phytochemical variation. Phytochemical variation in hybrids was identifiable and distinct from parentals due in part to transgressive variation in a subset of terpenoid compounds. Our results illustrate how history and environment predict ancestry variation across a hybrid zone, and how admixture generates novel phytochemical variation likely to have ecological consequences in a foundational tree species of the arid west.