Sweepstakes reproductive success via pervasive and recurrent selective sweeps

Area of Science:

• Population Genomics
• Evolutionary Biology
• Marine Ecology

Background:

• Highly fecund populations exhibit high early mortality, leading to rudimentary knowledge of recruitment dynamics.
• Understanding recruitment is vital for assessing genetic variation, population connectivity, local adaptation, and resilience.
• The sweepstakes reproductive success concept highlights variance in individual reproductive output, but its role in highly fecund organisms is debated.

Purpose of the Study:

• To determine if highly fecund organisms reproduce via sweepstakes.
• To investigate the relative roles of neutral versus selective sweepstakes in recruitment dynamics.
• To model recruitment dynamics in Atlantic cod using population genomic data.

Main Methods:

• Coalescent-based statistical analysis of population genomic data.
• Comparison of Kingman (no sweepstakes), Xi-Beta (random sweepstakes), and Durrett-Schweinsberg (selective sweepstakes) coalescent models.
• Inclusion of complex demographic factors and background selection in model fitting.

Main Results:

• Neither the Kingman nor the Xi-Beta coalescent models adequately fit the Atlantic cod population genomic data.
• The Durrett-Schweinsberg coalescent model, incorporating selective sweepstakes from recurrent new mutations, provided a superior explanation for the observed data.
• Selective sweepstakes are strongly implicated in explaining recruitment dynamics in this highly fecund species.

Conclusions:

• Models of sweepstakes reproduction and multiple-merger coalescents are essential for understanding genetic diversity in highly fecund populations.
• Selective sweepstakes, driven by new mutations, are a key mechanism shaping genetic diversity and recruitment in Atlantic cod.
• These findings have significant implications for fisheries stock management and the evolutionary genomics of high-fecundity species.