Abstract
Recombination has long been considered the primary mechanism to bring beneficial alleles together, which can increase the speed of adaptation from standing genetic variation. Recombination is fundamental to the transporter hypothesis proposed to explain precise parallel adaptation in Threespine Stickleback. We study an instance of freshwater adaptation in the Threespine Stickleback system using whole genome data from an evolutionary time-series to observe the genomic dynamics underlying rapid parallel adaptation. Here, we show that rapid adaptation to a freshwater environment depends on a few individuals with large haploblocks of freshwater-adaptive alleles (jackpot carriers) present among the anadromous founders at low frequencies. Biological kinship analyses indicates that mating among jackpot carriers and between jackpot carriers and non-jackpot individuals led to an increase in freshwater-adaptive alleles within the first few generations. This process allowed the population to overcome a substantial bottleneck likely caused by the low fitness of first-generation stickleback possessing a few freshwater-adaptive alleles born in the lake. Additionally, we find evidence that the genetic load that emerged from population growth after the bottleneck may have been reduced through an increase in homozygosity by inbreeding, ultimately purging deleterious alleles. Recombination likely played a limited role in this case of very rapid adaptation.
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Data availability
The whole genome data generated in this study have been deposited in the Sequence Read Archive (www.ncbi.nlm.nih.gov/sra) under accession code PRJNA1231081. Whole genomes from Rabbit Slough previously published in ref. 12 can be found at SRA under accession code PRJNA671690. All other whole genomes from ref. 12 can be found under accession code PRJNA247503. The data to generate the figures can be found in the Code Ocean capsule https://codeocean.com/capsule/9257557/tree (https://doi.org/10.24433/CO.2139373.v1).
Code availability
All custom scripts have been deposited to GitHub and can be accessed through the following link: https://github.com/a-kwakye/Rare-Jackpot-Individuals-Drive-Rapid-Adaptation-in-Threespine-Stickleback76 and Code Ocean at https://codeocean.com/capsule/9257557/tree (https://doi.org/10.24433/CO.2139373.v1).
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Acknowledgements
This work was supported by NIH R01GM124330 to K.R.V. and M.A.B., NSF grants DEB-0322818 and DEB-0919184 to M.A.B. and F. J. Rohlf, and the Newcomb College Institute of Tulane University to D.C.H. We would like to thank the many students who helped found the Scout Lake population and to capture stickleback from it. In particular, we thank W. E. Aguirre and P. J. Park, who were instrumental in the fieldwork. We thank members of the Veeramah Lab for comments and discussions during the preparation of this manuscript, especially Thomas Bertino and Rachael Herman for useful discussions on simulations.
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A.K: Formal analysis, DNA quantification, library preparation, genomic data processing; K.R: experimental design, DNA extraction, DNA quantification, library preparation, construction of reference panel for imputation, genomic data processing; M.W: crosses from Mile Lake; D.C.H: sampling, life-history data collection and processing; M.A.B: experimental design, population founding, most sampling, tissue sampling, and morphological data; K.R.V: experimental design, project supervision. A.K wrote the initial draft with input from all authors. All authors contributed to production of the final version.
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Kwakye, A., Reid, K., Wund, M.A. et al. Rare jackpot individuals drive rapid adaptation in Threespine Stickleback. Nat Commun (2026). https://doi.org/10.1038/s41467-026-71236-y
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DOI: https://doi.org/10.1038/s41467-026-71236-y
