Adaptation enables natural populations to survive in a changing environment. Understanding the mechanics of adaptation is therefore crucial for learning about the evolution and ecology of natural ...populations. We focus on the impact of random sweepstakes on selection in highly fecund haploid and diploid populations partitioned into two genetic types, with one type conferring selective advantage. For the diploid populations, we incorporate various dominance mechanisms. We assume that the populations may experience recurrent bottlenecks. In random sweepstakes, the distribution of individual recruitment success is highly skewed, resulting in a huge variance in the number of offspring contributed by the individuals present in any given generation. Using computer simulations, we investigate the joint effects of random sweepstakes, recurrent bottlenecks and dominance mechanisms on selection. In our framework, bottlenecks allow random sweepstakes to have an effect on the time to fixation, and in diploid populations, the effect of random sweepstakes depends on the dominance mechanism. We describe selective sweepstakes that are approximated by recurrent sweeps of strongly beneficial allelic types arising by mutation. We demonstrate that both types of sweepstakes reproduction may facilitate rapid adaptation (as defined based on the average time to fixation of a type conferring selective advantage conditioned on fixation of the type). However, whether random sweepstakes cause rapid adaptation depends also on their interactions with bottlenecks and dominance mechanisms. Finally, we review a case study in which a model of recurrent sweeps is shown to essentially explain population genomic data from Atlantic cod.
Evolutionary ecology may be described as explaining ecology through evolution and vice versa, but one may also view it as an integration of the two fields, where one takes the view that ecology and ...evolution are inseparable, and one can only begin to understand the biology of organisms by synthesizing the two fields. An example of such a synthesis is the biology of high fecundity and the associated concept of sweepstakes reproduction, or skewed individual recruitment success. As an illustration, we consider selection at linked sites under various dominance and epistasis mechanisms in a diploid population evolving according to random sweepstakes and experiencing recurrent bottlenecks. Using simulations, we give a few examples of the impact of the stated elements on selection. We show that depending on the dominance mechanisms, random sweepstakes can shorten the time to fixation (conditional on fixation) of the fit type at all sites. Bottlenecks tend to increase the fixation time, with random sweepstakes counteracting the effects of bottlenecks on the fixation time. Understanding the effect of random sweepstakes, recurrent bottlenecks, dominance mechanisms and epistasis on the fate of selectively advantageous mutations may help with explaining genetic diversity in natural highly fecund populations possibly evolving under sweepstakes reproduction.
We consider some genealogical properties of nested samples. The complete sample is assumed to have been drawn from a natural population characterised by high fecundity and sweepstakes reproduction ...(abbreviated HFSR). The random gene genealogies of the samples are—due to our assumption of HFSR—modelled by coalescent processes which admit multiple mergers of ancestral lineages looking back in time. Among the genealogical properties we consider are the probability that the most recent common ancestor is shared between the complete sample and the subsample nested within the complete sample; we also compare the lengths of ‘internal’ branches of nested genealogies between different coalescent processes. The results indicate how ‘informative’ a subsample is about the properties of the larger complete sample, how much information is gained by increasing the sample size, and how the ‘informativeness’ of the subsample varies between different coalescent processes.
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.
Abstract
Stochastic simulation is a key tool in population genetics, since the models involved are often analytically intractable and simulation is usually the only way of obtaining ground-truth data ...to evaluate inferences. Because of this, a large number of specialized simulation programs have been developed, each filling a particular niche, but with largely overlapping functionality and a substantial duplication of effort. Here, we introduce msprime version 1.0, which efficiently implements ancestry and mutation simulations based on the succinct tree sequence data structure and the tskit library. We summarize msprime’s many features, and show that its performance is excellent, often many times faster and more memory efficient than specialized alternatives. These high-performance features have been thoroughly tested and validated, and built using a collaborative, open source development model, which reduces duplication of effort and promotes software quality via community engagement.
Since its introduction in 2016, the msprime simulator has grown in popularity and is now one of the most commonly used tools in population genetics. This article marks the 1.0 release of msprime and summarizes the many features it has accumulated through an open source community development model. Despite its generality, msprime’s performance is excellent—in many cases orders of magnitude faster and more memory efficient than more specialized methods.
The ratio of singletons to the total number of segregating sites is used to estimate a reproduction parameter in a population model of large offspring numbers without having to jointly estimate the ...mutation rate. For neutral genetic variation, the ratio of singletons to the total number of segregating sites is equivalent to the ratio of total length of external branches to the total length of the gene genealogy. A multinomial maximum likelihood method that takes into account more frequency classes than just the singletons is developed to estimate the parameter of another large offspring number model. The performance of these methods with regard to sample size, mutation rate, and bias, is investigated by simulation. The expected value of the ratio of the total length of external branches to the total length of the whole tree is, using simulation, shown to decrease for the Kingman coalescent as sample size increases, but can increase or decrease, depending on parameter values, for
Λ
coalescents. Considering ratios of tree statistics, as opposed to considering lengths of various subtrees separately, can yield better insight into the dynamics of gene genealogies.
We report a complex set of scaling relationships between mutation and reproduction in a simple model of a population. These follow from a consideration of patterns of genetic diversity in a sample of ...DNA sequences. Five different possible limit processes, each with a different scaled mutation parameter, can be used to describe genetic diversity in a large population. Only one of these corresponds to the usual population genetic model, and the others make drastically different predictions about genetic diversity. The complexity arises because individuals can potentially have very many offspring. To the extent that this occurs in a given species, our results imply that inferences from genetic data made under the usual assumptions are likely to be wrong. Our results also uncover a fundamental difference between populations in which generations are overlapping and those in which generations are discrete. We choose one of the five limit processes that appears to be appropriate for some marine organisms and use a sample of genetic data from a population of Pacific oysters to infer the parameters of the model. The data suggest the presence of rare reproduction events in which approximately 8% of the population is replaced by the offspring of a single individual.
Natural highly fecund populations abound. These range from viruses to gadids. Many highly fecund populations are economically important. Highly fecund populations provide an important contrast to the ...low-fecundity organisms that have traditionally been applied in evolutionary studies. A key question regarding high fecundity is whether large numbers of offspring are produced on a regular basis, by few individuals each time, in a sweepstakes mode of reproduction. Such reproduction characteristics are not incorporated into the classical Wright-Fisher model, the standard reference model of population genetics, or similar types of models, in which each individual can produce only small numbers of offspring relative to the population size. The expected genomic footprints of population genetic models of sweepstakes reproduction are very different from those of the Wright-Fisher model. A key, immediate issue involves identifying the footprints of sweepstakes reproduction in genomic data. Whole-genome sequencing data can be used to distinguish the patterns made by sweepstakes reproduction from the patterns made by population growth in a population evolving according to the Wright-Fisher model (or similar models). If the hypothesis of sweepstakes reproduction cannot be rejected, then models of sweepstakes reproduction and associated multiple-merger coalescents will become at least as relevant as the Wright-Fisher model (or similar models) and the Kingman coalescent, the cornerstones of mathematical population genetics, in further discussions of evolutionary genomics of highly fecund populations.
Chaotic genetic patchiness （CGP） refers to surprising patterns of spatial and temporal genetic structure observed in some marine species at a scale where genetic variation should be efficiently ...homogenized by gene flow via larval dispersal. Here we review and discuss 4 mechanisms that could generate such unexpected patterns： selection, sweepstakes reproductive success, collective dispersal, and temporal shifts in local population dynamics. First, we review examples where genetic differentiation at specific loci was driven by diversifying selection, which was historically the first process invoked to explain CGP. Second, we turn to neutral demographic processes that may drive genome-wide effects, and whose effects on CGP may be enhanced when they act together. We discuss how sweepstakes reproductive success accelerates genetic drift and can thus generate genetic structure, provided that gene flow is not too strong. Collective dispersal is another mechanism whereby genetic structure can be maintained regardless of dispersal intensity, because it may prevent larval cohorts from becoming entirely mixed. Theoretical analyses of both the sweepstakes and the collective dispersal ideas are presented. Finally, we discuss an idea that has received less attention than the other ones just mentioned, namely temporal shifts in local population dynamics.
We consider a model of viability selection in a highly fecund haploid population with sweepstakes reproduction. We use simulations to estimate the time until the allelic type with highest fitness has ...reached high frequency in a finite population. We compare the time between two reproduction modes of high and low fecundity. We also consider the probability that the allelic type with highest fitness is lost from the population before reaching high frequency. Our simulation results indicate that highly fecund populations can evolve faster (in some cases much faster) than populations of low fecundity. However, high fecundity and sweepstakes reproduction also confer much higher risk of losing the allelic type with highest fitness from the population by chance. The impact of selection on driving alleles to high frequency varies depending on the trait value conferring highest fitness; in some cases the effect of selection can hardly be detected.
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