Adaptational lag to temperature in valley oak (Quercus lobata) can be mitigated by genome-informed assisted gene flow

Abstract

Climate change over the next century is predicted to cause widespread maladaptation in natural systems. This prediction, as well as many sustainable management and conservation practices, assumes that species are adapted to their current climate. However, this assumption is rarely tested. Using a large-scale common garden experiment combined with genome-wide sequencing, we found that valley oak (Quercus lobata), a foundational tree species in California ecosystems, showed a signature of adaptational lag to temperature, with fastest growth rates occurring at cooler temperatures than populations are currently experiencing. Future warming under realistic emissions scenarios was predicted to lead to further maladaptation to temperature and reduction in growth rates for valley oak. We then identified genotypes predicted to grow relatively fast under warmer temperatures and demonstrated that selecting seed sources based on their genotype has the potential to mitigate predicted negative consequences of future climate warming on growth rates in valley oak. These results illustrate that the belief of local adaptation underlying many management and conservation practices, such as using local seed sources for restoration, may not hold for some species. If contemporary adaptational lag is commonplace, we will need new approaches to help alleviate predicted negative consequences of climate warming on natural systems. We present one such approach, "genome-informed assisted gene flow," which optimally matches individuals to future climates based on genotype-phenotype-environment associations.

Keywords: adaptational lag; climate change; ecological genomics; local adaptation; temperature.

Fig. 1.

Effects of T_max difference on valley oak (Q. lobata) growth rate. (A) Conceptual diagram illustrating hypotheses of potential growth rate responses to T_max difference (i.e., temperature difference between site of planting and site of origin). (B) Predicted relative growth rates (i.e., growth relative to size) and approximate 95% confidence interval across T_max difference estimated from 2 common gardens. Dashed vertical line shows where planting site matches climate of origin (T_max difference = 0) and solid lines show T_max difference between Last Glacial Maximum 21,000 y ago and current climate (5.2° cooler) and predicted increase in temperature of 4.8 °C for rising emissions scenarios by 2100 (RCP 8.5).

Fig. 2.

Genotype-by-temperature interactions in valley oak (Q. lobata). (A) Predicted marginal effects of genotypes on relative growth rates of progeny planted into warmer temperatures estimated by genotype by T_max difference interactions of 12,357 SNPs across 12 chromosomes of valley oak. (B) Contrasting progeny growth responses for T_max difference and approximate 95% confidence intervals for maternal trees with GEBVs for optimal growth rate under warmer temperatures at the average value, +1 SD above average, and −1 SD below average. (C) Box plots showing observed adjusted relative growth rates for hypothetical sets of seedlings chosen randomly, or based on matching individuals to their future climate, matching individuals to future climate and accounting for adaptational lag in valley oak, or selecting maternal trees with high GEBVs.

Fig. 3.

Landscape distribution of predicted changes in relative growth rates for valley oak based on GEBVs. (A) Predicted changes in progeny relative growth rates by 2070 to 2099 under a business-as-usual emissions scenario (RCP 8.5) based on current distribution of maternal GEBVs across valley oak populations. Black circles indicate sampled localities. Black outlines indicate contemporary valley oak range. (B) Predicted changes in progeny relative growth rates by 2070 to 2099 for a scenario where maternal trees with the highest GEBV within 50 km of each planting site are used as a seed source.