Local to continental-scale variation in fitness and heritability in common bean

Authors: MACQUEEN, ALICE - University Of Texas At Austin; KHOURY, COLIN - International Center For Tropical Agriculture (CIAT); Miklas, Phillip - Phil; MCCLEAN, PHILLIP - North Dakota State University; OSORNO, JUAN - North Dakota State University; RUNCK, BRYAN - University Of Minnesota; WHITE, JEFFREY - University Of Florida; KANTAR, MICHAEL - University Of Hawaii; Neupane, Dhurba

Submitted to: Crop Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/14/2021
Publication Date: 2/2/2022
Citation: MacQueen, A.H., Khoury, C.K., Miklas, P.N., McClean, P.E., Osorno, J.M., Runck, B.C., White, J.W., Kantar, M.B., Ewing, P.M. 2022. Local to continental-scale variation in fitness and heritability in common bean. Crop Science. 62(2):767-779. https://doi.org/10.1002/csc2.20694.
DOI: https://doi.org/10.1002/csc2.20694

Interpretive Summary: Successful breeding programs balance tensions between reliable performance across environments vs excellent performance in specific locations while maintaining the genetic diversity needed to continue improving varieties. We quantified the outcomes of these tensions in dry bean, a globally important food crop with a unique history, using 35 years of continental-wide variety trials in the Cooperative Dry Bean Nursery (CDBN). Dry bean yields increased, but average annual yield increases were miniscule compared to yield benefits from local specialization as measured by the metric, "home field advantage". Moreover, selection efficiency as measured by increases in yield heritability, indicates an increase in genetic variation relative to environmental variation which is desirable for continued yield gains. A number of sites were identified that are conducive to efficient breeding of locally specialized varieties, which will allow rapid utilization of this "home field" strategy of variety improvement. These findings should assist bean breeders in developing cultivars with higher yields for target regions, ultimately benefiting producers and consumers.

Technical Abstract: Relative to natural populations, domesticated plant species undergo continuous selection for fitness across broad environmental gradients. This may alter how alleles conferring adaptation to local conditions segregate within populations. We quantified long-term improvement impacts on fitness (yield) heritability and fitness variation attributable to local adaptation with the metric, home field advantage, within common bean (Phaseolus vulgaris L.). We quantified patterns of adaptation breadth in 327 elite common bean entries planted across 70 sites in North America from 1981–2015 for the Cooperative Dry Bean Nursery (CDBN) trials. We also quantified patterns of heritability across sites and time to estimate the efficiency of selection for seed yield. Entries included representatives from three races and from both major genepools. These races have unique genetic structures and domestication histories, which we found corresponded to unique patterns of local adaptation and fitness heritability. The Durango and Mesoamerican races of the Middle American genepool both enjoyed higher-than-expected (p = 0.002) home field advantage, equal to up to 34 years of selection gains. The Nueva Granada race of the Andean genepool evidenced no local adaptation. Andean and Durango yields became more heritable across the study period (p < 0.001), but Mesoamerican fitness heritability decreased (p < 0.001). During improvement in the CDBN, we find agronomically significant increases in fitness attributable to local adaptation in the Middle American genepool. Surprisingly, we find that fitness heritability has increased over time in both genepools.