Highly fecund natural populations characterized by high early mortality abound, yet our knowledge about their recruitment dynamics is somewhat rudimentary. This knowledge gap has implications for our understanding of genetic variation, population connectivity, local adaptation, and the resilience of highly fecund populations. The concept of sweepstakes reproductive success, which posits a considerable variance and skew in individual reproductive output, is key to understanding the distribution of individual reproductive success. However, it still needs to be determined whether highly fecund organisms reproduce through sweepstakes and, if they do, the relative roles of neutral and selective sweepstakes. Here we use coalescent-based statistical analysis of population genomic data to show that selective sweepstakes likely explain recruitment dynamics in the highly fecund Atlantic cod. We show that the Kingman coalescent (modeling no sweepstakes) and the Xi-Beta coalescent (modeling random sweepstakes), including complex demography and background selection, do not provide an adequate fit for the data. The Durrett-Schweinsberg coalescent, in which selective sweepstakes result from recurrent and pervasive selective sweeps of new mutations, offers greater explanatory power. Our results show that models of sweepstakes reproduction and multiple-merger coalescents are relevant and necessary for understanding genetic diversity in highly fecund natural populations. These findings have fundamental implications for understanding the recruitment variation of fish stocks and general evolutionary genomics of high-fecundity organisms.

The data described in Árnason et al. 2023 are unfolded site frequency spectra of two populations of Atlantic cod (Gadus morhua) from Iceland. The site frequency spectra are estimated from whole-genome sequence results using ANGSD (Korneliussen et. al 2014). The estimation uses genotype likelihood (Samtools likelihood, gl1, and GATK likelihood, gl2) and returns 100 bootstrap estimates. An estimate is provided for each of the 23 chromosomes. Pacific cod (G. macrocephalus) was used as an outgroup to polarize the variation at sites.

Reference

Árnason E, Koskela J, Halldórsdóttir K, and Eldon B. 2023. Sweepstakes reproductive success via pervasive and recurrent selective sweeps. eLife 2023;12:e80781. DOI: https://doi.org/10.7554/eLife.80781.

Korneliussen TS, Albrechtsen A, Nielsen R. ANGSD: Analysis of Next Generation Sequencing Data. BMC Bioinformatics. 2014 nov; 15(1). http://dx.doi.org/10.1186/s12859-014-0356-4, doi: 10.1186/s12859-014-0356-4.

The data are presented as zipped archives of plain text files of site frequency spectrum and 100 bootstrap values for each chromosome and both likelihoods. The data are readable, for example, with R.