Sweepstakes reproductive success via pervasive and recurrent selective sweeps
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Evaluation Summary:
Analysis of molecular data from genome sequencing provides crucial information on the diversity of biological and evolutionary processes that shape genetic diversity. However, the models of genetic evolution used to make these inferences sometimes oversimplify important aspects of species biology. This study shows that accounting for high variance in reproductive success in models can better explain the genetic diversity of an extremely fecund marine species, the Atlantic cod. The manuscript is scientifically sound and provides careful statistical analyses of alternative evolutionary models. It concludes that pervasive selection, rather than demographic changes or sweepstakes reproduction, is one of the main drivers of genetic diversity in Atlantic cod.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 and Reviewer #3 agreed to share their name with the authors.)
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Abstract
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 (modelling no sweepstakes) and the Xi-Beta coalescent (modelling 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.
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Author Response
We thank the reviewers for their very thorough, detailed, and fair reviews that will help us improve the manuscript. We have two minor comments. First, we emphasize that the evidence is for pervasive positive selection being the main driver of the genetic diversity of Atlantic cod. Secondly, regarding the application of the Moran process to model the reproduction of high fecundity organisms. In the Moran process, a single individual is chosen at random to reproduce at any time, and another individual is chosen to die. However, the parent also persists in the population and can generate a large number of offspring in its lifetime. Hence, the Moran process does not imply an especially low level of fecundity. The multiple mergers seen in coalescent models of highly fecund organisms arise from a combination of high fecundity …
Author Response
We thank the reviewers for their very thorough, detailed, and fair reviews that will help us improve the manuscript. We have two minor comments. First, we emphasize that the evidence is for pervasive positive selection being the main driver of the genetic diversity of Atlantic cod. Secondly, regarding the application of the Moran process to model the reproduction of high fecundity organisms. In the Moran process, a single individual is chosen at random to reproduce at any time, and another individual is chosen to die. However, the parent also persists in the population and can generate a large number of offspring in its lifetime. Hence, the Moran process does not imply an especially low level of fecundity. The multiple mergers seen in coalescent models of highly fecund organisms arise from a combination of high fecundity and reproductive skew; models of high fecundity without skewness are consistent with genealogies with binary mergers only. Hence, the Durrett-Schweinsberg model we employ can be thought of as a model for a highly fecund organism for which reproductive skewness manifests through selective sweeps.
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Evaluation Summary:
Analysis of molecular data from genome sequencing provides crucial information on the diversity of biological and evolutionary processes that shape genetic diversity. However, the models of genetic evolution used to make these inferences sometimes oversimplify important aspects of species biology. This study shows that accounting for high variance in reproductive success in models can better explain the genetic diversity of an extremely fecund marine species, the Atlantic cod. The manuscript is scientifically sound and provides careful statistical analyses of alternative evolutionary models. It concludes that pervasive selection, rather than demographic changes or sweepstakes reproduction, is one of the main drivers of genetic diversity in Atlantic cod.
(This preprint has been reviewed by eLife. We include the public …
Evaluation Summary:
Analysis of molecular data from genome sequencing provides crucial information on the diversity of biological and evolutionary processes that shape genetic diversity. However, the models of genetic evolution used to make these inferences sometimes oversimplify important aspects of species biology. This study shows that accounting for high variance in reproductive success in models can better explain the genetic diversity of an extremely fecund marine species, the Atlantic cod. The manuscript is scientifically sound and provides careful statistical analyses of alternative evolutionary models. It concludes that pervasive selection, rather than demographic changes or sweepstakes reproduction, is one of the main drivers of genetic diversity in Atlantic cod.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 and Reviewer #3 agreed to share their name with the authors.)
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Reviewer #1 (Public Review):
The manuscript by Arnason et al. reports a careful in-depth analysis of genomic patterns of diversity of the Atlantic codfishes, sampled twice near the Icelandic coast. The manuscript is scientifically sound and provides thorough details of the statistical analysis and of the underlying models. In essence, the analysis demonstrates that recurrent selective sweeps are the most compatible scenario to explain the data. The analysis is extremely detailed, well constructed, and very convincing. It also advertises the family of Multiple-Merger Coalescents (MMCs) as good models for standard population genetics analyses. Overall, I found this article very interesting and extremely well-documented.
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Reviewer #2 (Public Review):
The genome-wide genetic diversity observed in samples of Atlantic cod does differ considerably from patterns expected under standard models of genetic diversity linked to Kingman's coalescent. One possible alternative explanation could be the presence of sweepstake reproductive success, where certain (ancestral) lineages dominate the sample's genealogy.
The manuscript shows clear evidence for the author's claim that the V-shape of the site frequency spectrum (SFS) from Atlantic cod Gadus morhua samples is a result of the population undergoing recurrent sweepstakes. However, not as previously thought via sweepstake mechanisms from a high fecundity - high early-life mortality mechanism, but via sweepstakes resulting from recurrent selective sweeps. The main tool for this essentially is a goodness-of-fit …
Reviewer #2 (Public Review):
The genome-wide genetic diversity observed in samples of Atlantic cod does differ considerably from patterns expected under standard models of genetic diversity linked to Kingman's coalescent. One possible alternative explanation could be the presence of sweepstake reproductive success, where certain (ancestral) lineages dominate the sample's genealogy.
The manuscript shows clear evidence for the author's claim that the V-shape of the site frequency spectrum (SFS) from Atlantic cod Gadus morhua samples is a result of the population undergoing recurrent sweepstakes. However, not as previously thought via sweepstake mechanisms from a high fecundity - high early-life mortality mechanism, but via sweepstakes resulting from recurrent selective sweeps. The main tool for this essentially is a goodness-of-fit approach (after parameter estimation within a parameterised model) that shows that the observed site frequency spectra (whole population, sub-populations, different SNP classes) cannot be explained by either model without pervasive selection and low to medium fecundity (which lead to Kingman's coalescent-like models) or with high fecundity - high random early-life mortality without selection (Xi-Beta-coalescent models), but are close to expectations of a multiple-merger coalescent model approximating a Moran model with high recombination and recurrent selective sweeps (the Durrett-Schweinsberg model, the "selective sweepstakes"). The authors do, in my opinion, a very good job of checking whether some further typical biological and demographic properties may explain the shape of the observed SFS (e.g. population structure) - which they convincingly reject. The results make a well-grounded case for selective sweepstakes being the main mechanism shaping genetic diversity in Atlantic cod. Since this is the first study linking a specific population/species to the Durrett-Schweinsberg model (DS model) of pervasive recurrent sweeps and thus legitimately establishing it as a viable model to consider when fitting to data, this has an impact well beyond Atlantic cod.
My only real, yet minor concern and disagreement with the authors is with their discussion point starting at line 531 on page 16: The authors argue that high fecundity does play a meaningful role in shaping the genetic diversity of Atlantic cod. However, the DS model is based on adding selective sweeps to a Moran model, a model clearly does not reflect high fecundity. While changing the underlying reproduction model in the DS model does not necessarily change the coalescent limit, it may do so or at least affect the time scale. Even the latter may affect some downstream results based on fitting the parameters of the DS model. While the arguments in this paragraph of the authors' discussion are not unreasonable per se, some more care should be taken to reconcile these with the assumptions of the DS model.
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Reviewer #3 (Public Review):
This study addresses fundamental aspects of the eco-evolutionary dynamics of highly fecund organisms experiencing huge mortality rates during early life stages. In such species, a mechanism called "sweepstakes reproductive success" (Hedgecock, 1994) has been proposed to understand the dynamics of recruitment, in which individual reproductive success shows high variance and skewed distribution. Sweepstakes reproductive success can be either neutral due to random environmental variation influencing the recruitment of reproducing offspring, or selective because genetic variation at particular loci influences the likelihood of successful recruitment. Unfortunately, empirical tests of sweepstakes reproduction remain scarce due to the difficulty of studying individual reproductive success directly, particularly in …
Reviewer #3 (Public Review):
This study addresses fundamental aspects of the eco-evolutionary dynamics of highly fecund organisms experiencing huge mortality rates during early life stages. In such species, a mechanism called "sweepstakes reproductive success" (Hedgecock, 1994) has been proposed to understand the dynamics of recruitment, in which individual reproductive success shows high variance and skewed distribution. Sweepstakes reproductive success can be either neutral due to random environmental variation influencing the recruitment of reproducing offspring, or selective because genetic variation at particular loci influences the likelihood of successful recruitment. Unfortunately, empirical tests of sweepstakes reproduction remain scarce due to the difficulty of studying individual reproductive success directly, particularly in highly fecund marine organisms.
By analysing genome-wide genetic diversity data under different coalescent models representing alternative recruitment dynamics, this pioneering study specifically tests whether random or selective sweepstakes reproduction occurs in the highly fecund Atlantic cod. Using the classical Kingman coalescent and two multiple-merger coalescent models approximating random sweepstakes (the Xi-Beta-coalescent model) and selective sweepstakes (the Durrett-Schweinsberg model), the authors show that genetic diversity in the Atlantic cod genome is most likely shaped by pervasive selective sweeps of new beneficial mutations. The best-fit selective sweepstakes model is able to reproduce the main characteristics of the allele frequency spectrum of each Atlantic cod population, while alternative models include either random sweepstakes or other biologically plausible scenarios (i.e. historical demographic changes, cryptic breeding structure, and background selection) show a much poorer fit.
These findings have a broad impact on evolutionary genomics since they provide a new and exciting perspective on the choice of appropriate coalescent models for the study of highly fecund organisms that may experience high rates of selective mortality during early life stages. The low-fecundity low-variance reproductive success model classically used in evolutionary genetics may simply not apply in highly fecund organisms with skewed offspring distribution.
By confronting different alternative models of coalescence with genome-scale genetic diversity data, this work provides a roadmap for exploring fundamental processes at the crossroads between ecology and evolution. It highlights the importance of (i) understanding the potential impact of species-specific biological characteristics when inferring demography and selection from molecular data, and (ii) being aware of the potentially significant effects of unaccounted aspects of the data (e.g. variant misorientation, past admixture) on the interpretation of results.
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