Genome-wide shifts in climate-related variation underpin responses to selective breeding in a widespread conifer

Locally adapted temperate tree populations exhibit genetic trade-offs
among climate-related traits that can be exacerbated by selective
breeding, and are challenging to manage under climate change. To inform
climatically adaptive forest management, we investigated the genetic
architecture and impacts of selective breeding on four climate-related
traits in 105 natural and 20 selectively bred lodgepole pine populations
from western Canada. Growth, cold injury and growth initiation and growth
cessation phenotypes were tested for associations with 18,600 SNPs in
natural populations to identify ‘positive effect alleles’ (PEAs). The
effects of artificial selection for faster growth on PEA frequencies for
each trait were quantified in breeding populations from different
climates. Substantial shifts in PEA proportions and frequencies were
observed across many loci after two generations of selective breeding for
height, and responses of phenology-associated PEAs differed strongly among
climatic regions. Extensive genetic overlap was evident among traits.
Alleles most strongly associated with greater height were often also
associated with greater cold injury and delayed phenology, although it is
unclear whether potential trade-offs arose directly from pleiotropy or
indirectly via genetic linkage. Modest variation among populations in PEA
frequencies across many loci was associated with large phenotypic
differences and strong climatic gradients, providing support for assisted
gene flow polices. Relationships among genotypes, phenotypes and climate
in natural populations were maintained or strengthened by selective
breeding. However, future adaptive phenotypes and assisted gene flow may
be compromised if selective breeding further increases the PEA frequencies
of SNPs involved in adaptive trade-offs among climate-related traits.