Reproductive isolation of hybrid populations driven by genetic incompatibilities

Reproductive isolation of hybrid populations driven by genetic incompatibilities

Molly Schumer, Rongfeng Cui, Gil G Rosenthal, Peter Andolfatto
doi: http://dx.doi.org/10.1101/007518

Despite its role in homogenizing populations, hybridization has also been proposed as a means to generate new species. The conceptual basis for this idea is that hybridization can result in novel phenotypes through recombination between the parental genomes, allowing a hybrid population to occupy ecological niches unavailable to parental species. A key feature of these models is that these novel phenotypes ecologically isolate hybrid populations from parental populations, precipitating speciation. Here we present an alternative model of the evolution of reproductive isolation in hybrid populations that occurs as a simple consequence of selection against incompatibilities. Unlike previous models, our model does not require small population sizes, the availability of new niches for hybrids or ecological or sexual selection on hybrid traits. We show that reproductive isolation between hybrids and parents evolves frequently and rapidly under this model, even in the presence of ongoing migration with parental species and strong selection against hybrids. Our model predicts that multiple distinct hybrid species can emerge from replicate hybrid populations formed from the same parental species, potentially generating patterns of species diversity and relatedness that mimic adaptive radiations.

Clonal interference and Muller’s ratchet in spatial habitats

Clonal interference and Muller’s ratchet in spatial habitats
Jakub Otwinowski, Joachim Krug
(Submitted on 18 Feb 2013 (v1), last revised 23 Jul 2014 (this version, v3))

Competition between independently arising beneficial mutations is enhanced in spatial populations due to the linear rather than exponential growth of clones. Recent theoretical studies have pointed out that the resulting fitness dynamics is analogous to a surface growth process, where new layers nucleate and spread stochastically, leading to the build up of scale-invariant roughness. This scenario differs qualitatively from the standard view of adaptation in that the speed of adaptation becomes independent of population size while the fitness variance does not. Here we exploit recent progress in the understanding of surface growth processes to obtain precise predictions for the universal, non-Gaussian shape of the fitness distribution for one-dimensional habitats, which are verified by simulations. When the mutations are deleterious rather than beneficial the problem becomes a spatial version of Muller’s ratchet. In contrast to the case of well-mixed populations, the rate of fitness decline remains finite even in the limit of an infinite habitat, provided the ratio Ud/s2 between the deleterious mutation rate and the square of the (negative) selection coefficient is sufficiently large. Using again an analogy to surface growth models we show that the transition between the stationary and the moving state of the ratchet is governed by directed percolation.

Fixation properties of subdivided populations with balancing selection


Fixation properties of subdivided populations with balancing selection

Pierangelo Lombardo, Andrea Gambassi, Luca Dall’Asta
Comments: 17 pages, 10 figures
Subjects: Populations and Evolution (q-bio.PE); Statistical Mechanics (cond-mat.stat-mech); Biological Physics (physics.bio-ph)

In subdivided populations, migration acts together with selection and genetic drift and determines their evolution. Building up on a recently proposed method, which hinges on the emergence of a time scale separation between local and global dynamics, we study the fixation properties of subdivided populations in the presence of balancing selection. The approximation implied by the method is accurate when the effective selection strength is small and the number of subpopulations is large. In particular, it predicts a phase transition between species coexistence and biodiversity loss in the infinite-size limit and, in finite populations, a nonmonotonic dependence of the mean fixation time on the migration rate. In order to investigate the fixation properties of the subdivided population for stronger selection, we introduce an effective coarser description of the dynamics in terms of a voter model with intermediate states, which highlights the basic mechanisms driving the evolutionary process.

Stress-Induced Mutagenesis and Complex Adaptation

Stress-Induced Mutagenesis and Complex Adaptation
Yoav Ram, Lilach Hadany
(Submitted on 14 Jul 2014)

Because mutations are mostly deleterious, mutation rates should be reduced by natural selection. However, mutations also provide the raw material for adaptation. Therefore, evolutionary theory suggests that the mutation rate must balance between adaptability – the ability to adapt – and adaptedness – the ability to remain adapted. We model an asexual population crossing a fitness valley and analyze the rate of complex adaptation with and without stress-induced mutagenesis – the increase of mutation rates in response to stress or maladaptation. We show that stress-induced mutagenesis increases the rate of complex adaptation without reducing the population mean fitness, thus breaking the evolutionary trade-off between adaptability and adaptedness. Our theoretical results support the hypothesis that stress-induced mutagenesis promotes adaptation and provide quantitative predictions of the rate of complex adaptation with different mutational strategies.

On the number of ranked species trees producing anomalous ranked gene trees

On the number of ranked species trees producing anomalous ranked gene trees
Filippo Disanto, Noah A. Rosenberg
Subjects: Populations and Evolution (q-bio.PE)

Analysis of probability distributions conditional on species trees has demonstrated the existence of anomalous ranked gene trees (ARGTs), ranked gene trees that are more probable than the ranked gene tree that accords with the ranked species tree. Here, to improve the characterization of ARGTs, we study enumerative and probabilistic properties of two classes of ranked labeled species trees, focusing on the presence or avoidance of certain subtree patterns associated with the production of ARGTs. We provide exact enumerations and asymptotic estimates for cardinalities of these sets of trees, showing that as the number of species increases without bound, the fraction of all ranked labeled species trees that are ARGT-producing approaches 1. This result extends beyond earlier existence results to provide a probabilistic claim about the frequency of ARGTs.

The site frequency spectrum of dispensable genes

The site frequency spectrum of dispensable genes
Franz Baumdicker
Comments: 24 pages, 8 figures
Subjects: Populations and Evolution (q-bio.PE); Probability (math.PR)

The differences between DNA-sequences within a population are the basis to infer the ancestral relationship of the individuals. Within the classical infinitely many sites model, it is possible to estimate the mutation rate based on the site frequency spectrum, which is comprised by the numbers $C_1,…,C_{n-1}$, where n is the sample size and $C_s$ is the number of site mutations (Single Nucleotide Polymorphisms, SNPs) which are seen in $s$ genomes. Classical results can be used to compare the observed site frequency spectrum with its neutral expectation, $E[C_s]= \theta_2/s$, where $\theta_2$ is the scaled site mutation rate. In this paper, we will relax the assumption of the infinitely many sites model that all individuals only carry homologous genetic material. Especially, it is today well-known that bacterial genomes have the ability to gain and lose genes, such that every single genome is a mosaic of genes, and genes are present and absent in a random fashion, giving rise to the dispensable genome. While this presence and absence has been modeled under neutral evolution within the infinitely many genes model in previous papers, we link presence and absence of genes with the numbers of site mutations seen within each gene. In this work we derive a formula for the expectation of the joint gene and site frequency spectrum, denotes $G_{k,s}$ the number of mutated sites occurring in exactly $s$ gene sequences, while the corresponding gene is present in exactly $k$ individuals. We show that standard estimators of $\theta_2$ for dispensable genes are biased and that the site frequency spectrum for dispensable genes differs from the classical result.

Convergent Evolution During Local Adaptation to Patchy Landscapes

Convergent Evolution During Local Adaptation to Patchy Landscapes
Peter L. Ralph, Graham Coop

Species often encounter, and adapt to, many patches of locally similar environmental conditions across their range. Such adaptation can occur through convergent evolution as different alleles arise and spread in different patches, or through the spread of alleles by migration acting to synchronize adaptation across the species. The tension between the two reflects the degree of constraint imposed on evolution by the underlying genetic architecture versus how how effectively selection acts to inhibit the geographic spread of locally adapted alleles. This paper studies a model of the balance between these two routes to adaptation in continuous environments with patchy selection pressures. We address the following questions: How long does it take for a new, locally adapted allele to appear in a patch of habitat where it is favored through new mutation? Or, through migration from another, already adapted patch? Which is more likely to occur, as a function of distance between the patches? How can we tell which has occurred, i.e.\ what population genetic signal is left by the spread of migrant alleles and how long does this signal persist for? To answer these questions we decompose the migration–selection equilibrium surrounding an already adapted patch into families of migrant alleles, in particular treating those rare families that reach new patches as spatial branching processes. This provides a way to understand the role of geographic separation between patches in promoting convergent adaptation and the genomic signals it leaves behind. We illustrate these ideas using the convergent evolution of cryptic coloration in the rock pocket mouse, Chaetodipus intermedius, as an empirical example.

Purifying selection, drift and reversible mutation with arbitrarily high mutation rates


Purifying selection, drift and reversible mutation with arbitrarily high mutation rates

Brian Charlesworth, Kavita Jain
Comments: Supplementary Information available on request
Subjects: Populations and Evolution (q-bio.PE)

Some species exhibit very high levels of DNA sequence variability; there is also evidence for the existence of heritable epigenetic variants that experience state changes at a much higher rate than sequence variants. In both cases, the resulting high diversity levels within a population (hyperdiversity) mean that standard population genetics methods are not trustworthy. We analyze a population genetics model that incorporates purifying selection, reversible mutations and genetic drift, assuming a stationary population size. We derive analytical results for both population parameters and sample statistics, and discuss their implications for studies of natural genetic and epigenetic variation. In particular, we find that (1) many more intermediate frequency variants are expected than under standard models, even with moderately strong purifying selection (2) rates of evolution under purifying selection may be close to, or even exceed, neutral rates. These findings are related to empirical studies of sequence and epigenetic variation.

The effective founder effect in a spatially expanding population

The effective founder effect in a spatially expanding population
Benjamin Marco Peter, Montgomery Slatkin

The gradual loss of diversity associated with range expansions is a well known pattern observed in many species, and can be explained with a serial founder model. We show that under a branching process approximation, this loss in diversity is due to the difference in offspring variance between individuals at and away from the expansion front, which allows us to measure the strength of the founder effect, dependant on an effective founder size. We demonstrate that the predictions from the branching process model fit very well with Wright-Fisher forward simulations and backwards simulations under a modified Kingman coalescent, and further show that estimates of the effective founder size are robust to possibly confounding factors such as migration between subpopulations. We apply our method to a data set of Arabidopsis thaliana, where we find that the founder effect is about three times stronger in the Americas than in Europe, which may be attributed to the more recent, faster expansion.

Autosomal admixture levels are informative about sex bias in admixed populations

Autosomal admixture levels are informative about sex bias in admixed populations

Amy Goldberg, Paul Verdu, Noah A Rosenberg

Sex-biased admixture has been observed in a wide variety of admixed populations. Genetic variation in sex chromosomes and ratios of quantities computed from sex chromosomes and autosomes have often been examined in order to infer patterns of sex-biased admixture, typically using statistical approaches that do not mechanistically model the complexity of a sex-specific history of admixture. Here, expanding on a model of Verdu \& Rosenberg (2011) that did not include sex specificity, we develop a model that mechanistically examines sex-specific admixture histories. Under the model, multiple source populations contribute to an admixed population, potentially with their male and female contributions varying over time. In an admixed population descended from two source groups, we derive the moments of the distribution of the autosomal admixture fraction from a specific source population as a function of sex-specific introgression parameters and time. Considering admixture processes that are constant in time, we demonstrate that surprisingly, although the mean autosomal admixture fraction from a specific source population does not reveal a sex bias in the admixture history, the variance of autosomal admixture is informative about sex bias. Specifically, the long-term variance decreases as the sex bias from a contributing source population increases. This result can be viewed as analogous to the reduction in effective population size for populations with an unequal number of breeding males and females. Our approach can contribute to methods for inference of the history of complex sex-biased admixture processes by enabling consideration of the effect of sex-biased admixture on autosomal DNA.