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Reproductive isolation of hybrid populations driven by genetic incompatibilities.

Schumer M, Cui R, Rosenthal GG, Andolfatto P - PLoS Genet. (2015)

Bottom Line: 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.This non-adaptive process can therefore generate patterns of species diversity and relatedness that resemble an adaptive radiation.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey, United States of America.

ABSTRACT
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. Here we present an alternative model of the evolution of reproductive isolation in hybrid populations that occurs as a simple consequence of selection against genetic incompatibilities. Unlike previous models of hybrid speciation, our model does not incorporate inbreeding, or assume that hybrids have an ecological or reproductive fitness advantage relative to parental populations. We show that reproductive isolation between hybrids and parental species can evolve frequently and rapidly under this model, even in the presence of substantial ongoing immigration from parental species and strong selection against hybrids. An interesting prediction of our model is that replicate hybrid populations formed from the same pair of parental species can evolve reproductive isolation from each other. This non-adaptive process can therefore generate patterns of species diversity and relatedness that resemble an adaptive radiation. Intriguingly, several known hybrid species exhibit patterns of reproductive isolation consistent with the predictions of our model.

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Hybrid populations rapidly fix for hybrid incompatibility locus pairs.Selection drives hybrid incompatibility loci to fixation, even when a hybrid population forms at equal admixture proportions (f = 0.5). Black lines show average parent 1 ancestry at a hybrid incompatibility pair (h = 0.5, s = 0.1) in 50 replicate populations of (A) N = 1,000 or (B) N = 10,000 diploid individuals. Gray lines show results for this same population size with no selection. Because of this behavior, two incompatibility pairs may fix for opposite parents, resulting in reproductive isolation of hybrids from both parents (see Fig. 1).
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pgen.1005041.g002: Hybrid populations rapidly fix for hybrid incompatibility locus pairs.Selection drives hybrid incompatibility loci to fixation, even when a hybrid population forms at equal admixture proportions (f = 0.5). Black lines show average parent 1 ancestry at a hybrid incompatibility pair (h = 0.5, s = 0.1) in 50 replicate populations of (A) N = 1,000 or (B) N = 10,000 diploid individuals. Gray lines show results for this same population size with no selection. Because of this behavior, two incompatibility pairs may fix for opposite parents, resulting in reproductive isolation of hybrids from both parents (see Fig. 1).

Mentions: This purely deterministic model of selection on hybrid incompatibilities is unrealistic because even large populations experience some degree of genetic drift. We thus extended the model to include genetic drift, which can affect the speed and direction of fixation of incompatibility pairs (S5 Fig.). For neutral BDM incompatibilities (S1 Fig.), this model does not predict fixation of genotypes incompatible with either parental species (S4 Fig.). In contrast, for coevolving or adaptive BDM incompatibilities (S1 Text, S1 and S2 Figs), the two-locus finite population model predicts that at equal admixture proportions (f = 0.5), a single incompatibility pair has a 50% chance of fixing for either parental allele combination (Fig. 2, S2 Text, S1 Table). Interestingly, while genetic drift in small populations could accomplish the same thing (9), the process described here occurs rapidly in large populations and is driven by deterministic selection (Fig. 2). Given these dynamics, it is clear that large hybrid populations with two or more of these types of hybrid incompatibilities could, in principle, fix for one parental genotype at one incompatibility pair and the other parental genotype at the other incompatibility pair (Fig. 1). This outcome would result in reproductive isolation of the hybrid population from both parental species. With two codominant incompatibility pairs and equal admixture proportions, the probability that a hybrid population will become isolated can be predicted by a simple binomial. However the binomial prediction breaks down when there is variation in dominance, admixture proportions, or linkage between incompatibilities, and thus we explore these further by simulation.


Reproductive isolation of hybrid populations driven by genetic incompatibilities.

Schumer M, Cui R, Rosenthal GG, Andolfatto P - PLoS Genet. (2015)

Hybrid populations rapidly fix for hybrid incompatibility locus pairs.Selection drives hybrid incompatibility loci to fixation, even when a hybrid population forms at equal admixture proportions (f = 0.5). Black lines show average parent 1 ancestry at a hybrid incompatibility pair (h = 0.5, s = 0.1) in 50 replicate populations of (A) N = 1,000 or (B) N = 10,000 diploid individuals. Gray lines show results for this same population size with no selection. Because of this behavior, two incompatibility pairs may fix for opposite parents, resulting in reproductive isolation of hybrids from both parents (see Fig. 1).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4359097&req=5

pgen.1005041.g002: Hybrid populations rapidly fix for hybrid incompatibility locus pairs.Selection drives hybrid incompatibility loci to fixation, even when a hybrid population forms at equal admixture proportions (f = 0.5). Black lines show average parent 1 ancestry at a hybrid incompatibility pair (h = 0.5, s = 0.1) in 50 replicate populations of (A) N = 1,000 or (B) N = 10,000 diploid individuals. Gray lines show results for this same population size with no selection. Because of this behavior, two incompatibility pairs may fix for opposite parents, resulting in reproductive isolation of hybrids from both parents (see Fig. 1).
Mentions: This purely deterministic model of selection on hybrid incompatibilities is unrealistic because even large populations experience some degree of genetic drift. We thus extended the model to include genetic drift, which can affect the speed and direction of fixation of incompatibility pairs (S5 Fig.). For neutral BDM incompatibilities (S1 Fig.), this model does not predict fixation of genotypes incompatible with either parental species (S4 Fig.). In contrast, for coevolving or adaptive BDM incompatibilities (S1 Text, S1 and S2 Figs), the two-locus finite population model predicts that at equal admixture proportions (f = 0.5), a single incompatibility pair has a 50% chance of fixing for either parental allele combination (Fig. 2, S2 Text, S1 Table). Interestingly, while genetic drift in small populations could accomplish the same thing (9), the process described here occurs rapidly in large populations and is driven by deterministic selection (Fig. 2). Given these dynamics, it is clear that large hybrid populations with two or more of these types of hybrid incompatibilities could, in principle, fix for one parental genotype at one incompatibility pair and the other parental genotype at the other incompatibility pair (Fig. 1). This outcome would result in reproductive isolation of the hybrid population from both parental species. With two codominant incompatibility pairs and equal admixture proportions, the probability that a hybrid population will become isolated can be predicted by a simple binomial. However the binomial prediction breaks down when there is variation in dominance, admixture proportions, or linkage between incompatibilities, and thus we explore these further by simulation.

Bottom Line: 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.This non-adaptive process can therefore generate patterns of species diversity and relatedness that resemble an adaptive radiation.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey, United States of America.

ABSTRACT
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. Here we present an alternative model of the evolution of reproductive isolation in hybrid populations that occurs as a simple consequence of selection against genetic incompatibilities. Unlike previous models of hybrid speciation, our model does not incorporate inbreeding, or assume that hybrids have an ecological or reproductive fitness advantage relative to parental populations. We show that reproductive isolation between hybrids and parental species can evolve frequently and rapidly under this model, even in the presence of substantial ongoing immigration from parental species and strong selection against hybrids. An interesting prediction of our model is that replicate hybrid populations formed from the same pair of parental species can evolve reproductive isolation from each other. This non-adaptive process can therefore generate patterns of species diversity and relatedness that resemble an adaptive radiation. Intriguingly, several known hybrid species exhibit patterns of reproductive isolation consistent with the predictions of our model.

Show MeSH