Powerful detection of polygenic selection and environmental adaptation in US beef cattle populations

Abstract

Selection on complex traits can rapidly drive evolution, especially in stressful environments. This polygenic selection does not leave intense sweep signatures on the genome, rather many loci experience small allele frequency shifts, resulting in large cumulative phenotypic changes. Directional selection and local adaptation are actively changing populations; but, identifying loci underlying polygenic or environmental selection has been difficult. We use genomic data on tens of thousands of cattle from three populations, distributed over time and landscapes, in linear mixed models with novel dependent variables to map signatures of selection on complex traits and local adaptation. We identify 207 genomic loci associated with an animals birth date, representing ongoing selection for monogenic and polygenic traits. Additionally, hundreds of additional loci are associated with continuous and discrete environments, providing evidence for local adaptation. These candidate loci highlight the nervous systems possible role in local adaptation. While advanced technologies have increased the rate of directional selection in cattle, it has likely been at the expense of historically generated local adaptation, which is especially problematic in changing climates. When applied to large, diverse cattle datasets, these selection mapping methods provide an insight into how selection on complex traits continually shapes the genome. Further, by understanding the genomic loci implicated in adaptation, may help us breed more adapted and efficient cattle and begin understanding the basis for mammalian adaptation, especially in changing climates. These selection mapping approaches help clarify selective forces and loci in evolutionary, model, and agricultural contexts. Author SummaryInterest in mapping the impacts of selection and local adaptation on the genome is increasing due to the novel stressors presented by climate change. Until now, approaches have largely focused on mapping "sweeps" on large-effect loci. Highly powered datasets that are both temporally and geographically distributed have not existed. Recently, large numbers of beef cattle have been genotyped across the United States, including influential individuals with cryopreserved semen. This has created multiple powerful datasets distributed over time and landscapes. Here, we map the recent effects of selection and local adaptation in three cattle populations. The results provide insight into the biology of mammalian adaptation and generate useful tools for selecting and breeding better-adapted cattle for a changing environment.