Growth gains from selective breeding in a spruce hybrid zone do not compromise local adaptation to climate.

Hybrid zones contain extensive standing genetic variation that facilitates rapid responses to selection. The ×  hybrid zone in western Canada is the focus of tree breeding programs that annually produce ~90 million reforestation seedlings. Understanding the direct and indirect effects of selective breeding on adaptive variation is necessary to implement assisted gene flow (AGF) polices in Alberta and British Columbia that match these seedlings with future climates. We decomposed relationships among hybrid ancestry, adaptive traits, and climate to understand the implications of selective breeding for climate adaptations and AGF strategies. The effects of selection on associations among hybrid index estimated from ~6,500 SNPs, adaptive traits, and provenance climates were assessed for ~2,400 common garden seedlings. Hybrid index differences between natural and selected seedlings within breeding zones were small in Alberta (average +2%), but larger and more variable in BC (average -7%, range -24% to +1%), slightly favoring ancestry. The average height growth gain of selected seedlings over natural seedlings within breeding zones was 36% (range 12%-86%). Clines in growth with temperature-related variables were strong, but differed little between selected and natural populations. Seedling hybrid index and growth trait associations with evapotranspiration-related climate variables were stronger in selected than in natural seedlings, indicating possible preadaptation to drier future climates. Associations among cold hardiness, hybrid ancestry, and cold-related climate variables dominated signals of local adaptation and were preserved in breeding populations. Strong hybrid ancestry-phenotype-climate associations suggest that AGF will be necessary to match interior spruce breeding populations with shifting future climates. The absence of antagonistic selection responses among traits and maintenance of cold adaptation in selected seedlings suggests breeding populations can be safely redeployed using AGF prescriptions similar to those of natural populations.