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Comparing phenotypic and genetic variation in California walnuts (Juglans californica and J. hindsii) to resolve species identities and scan for climate adaptations

Abstract

Juglans californica and J. hindsii are sister taxa endemic to California with significant economic, ecological, and cultural relevance to the state. Each taxon is a foundation species for a rare and threatened plant community, the walnut woodland, in their respective regions. Both species are distributed throughout much of California, but their species identities still need clarification due to some authorities' treatment of both taxa as subspecies of Juglans californica. The future of either taxon will need to confront climate change within a highly urbanized and fragmented landscape, where the usual options for long-living tree species are to adapt, disperse, or die, but landscape genomic-based predictions cannot occur without a clear understanding of how each taxon is genetically and ecologically distinct. Using herbarium specimens and whole-genome sequences for 104 field-identified Juglans californica sampled throughout California, we describe spatially explicit patterns of leaf morphology, genetic structure, and genetic diversity in both taxa and leverage genetic-environment associations to describe distinct patterns of local adaptation that corroborate that these taxa are should be treated as different species. Genetic structure analyses suggest that J. californica is restricted to the Los Angeles Metropolitan area and the Transverse Ranges. J. hindsii occurs throughout much of Northern California and extends into the southmost portion of the species range in San Diego County. Hybridization with a third cluster occurs throughout both of the species. Leaf trait values, including abaxial vein axil hair area, leaflet number, and petiole length, significantly differ between species and corroborate genetic structure results. J. hindsii has higher genetic diversity than J. californica (nucleotide diversity, biallelic richness, and observed heterozygosity) and local adaptation patterns strongly influenced by winter bioclimatic variables based on GEA analyses. J. californica has local adaptation patterns that are strongly influenced by summer temperature and water availability. These results suggest that each species may respond differently to climate change projections and require species-specific protections against ongoing habitat loss and climate change.

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