Genomic signature of reproductive isolation between the last two remnant populations of Torrey pine ( Pinus torreyana Parry)

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Abstract

Understanding the genomic mechanisms contributing to speciation requires studies of taxa that are in the early stages of divergence, before complete reproductive isolation has evolved. One of the rarest pines in the world, Torrey Pine ( Pinus torreyana Parry), persists naturally across one island and one mainland population in southern California, and is an ideal system for assessing the evolution of divergence as they are morphologically and genetically differentiated, but experience some connectivity. Using ddRADseq and GWAS for a common garden experiment of island, mainland, and F1 genotypes, we identified divergent loci, their function, and their relationship to variation in fitness. Simulating neutral evolution and admixture, loci were identified that were more differentiated than expected and exhibited reduced admixture in the F1s. SNPs with reduced admixture were enriched for reproductive-related functions, such as growth and pollination. Additionally, one locus strongly associated with differential fitness exhibited reduced admixture, suggesting it could be involved in promoting reproductive isolation. With persistent genomic signatures of the evolution of reproductive isolation, Torrey pine may be at the early stages of speciation. As Torrey pine is a candidate for interpopulation genetic rescue, caution is warranted where longer-term gene flow between diverged populations may result in reduced fitness if barriers have evolved.

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