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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 develop reproductive isolation from both parental species, even in the presence of migration.Once hybrid populations diverge in ancestry at hybrid incompatibility loci from parental populations, individual hybrids have higher fitness on average when they mate with other hybrids in their population compared to either parent. (A) No migration and (B) ongoing migration (4Nm1 = 4Nm2 = 8) from parental populations. Dark points represent the mean fitness, and smears represent the means of 1,000 bootstrap samples. In B, fitness is normalized to the mean fitness of individuals in the parental populations. Simulation parameters: 100 replicates per time point, N = 1000, 20 hybrid incompatibility pairs, s1, s2 and h drawn from distributions (exponential, exponential and uniform, respectively, see details S5 Text).
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pgen.1005041.g004: Hybrid populations rapidly develop reproductive isolation from both parental species, even in the presence of migration.Once hybrid populations diverge in ancestry at hybrid incompatibility loci from parental populations, individual hybrids have higher fitness on average when they mate with other hybrids in their population compared to either parent. (A) No migration and (B) ongoing migration (4Nm1 = 4Nm2 = 8) from parental populations. Dark points represent the mean fitness, and smears represent the means of 1,000 bootstrap samples. In B, fitness is normalized to the mean fitness of individuals in the parental populations. Simulation parameters: 100 replicates per time point, N = 1000, 20 hybrid incompatibility pairs, s1, s2 and h drawn from distributions (exponential, exponential and uniform, respectively, see details S5 Text).

Mentions: The above simulations focus on simple models that show this process can occur in principle. To capture more biological realism in the number and types of incompatibilities, we simulated 20 incompatibility pairs with randomly determined genomic position and dominance, exponentially distributed selection coefficients (mean s = 0.05) and variation in asymmetry of selection (see above and S5 Text). In these simulations, 95% of populations developed isolation from both parental species. On average, the hybrid population first evolved isolation from both parental species after ~250 generations and was isolated from each by 7 incompatibility pairs within 1000 generations. Since incompatibility pairs with the largest fitness effects tend to fix first, hybrid populations developed considerable reproductive isolation from parental species even before all incompatibilities were fixed in the population (Figs. 4 and S11). Overall, our simulations suggest that rapid evolution of reproductive isolation of hybrid populations is likely when parental species are separated by several hybrid incompatibility pairs.


Reproductive isolation of hybrid populations driven by genetic incompatibilities.

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

Hybrid populations rapidly develop reproductive isolation from both parental species, even in the presence of migration.Once hybrid populations diverge in ancestry at hybrid incompatibility loci from parental populations, individual hybrids have higher fitness on average when they mate with other hybrids in their population compared to either parent. (A) No migration and (B) ongoing migration (4Nm1 = 4Nm2 = 8) from parental populations. Dark points represent the mean fitness, and smears represent the means of 1,000 bootstrap samples. In B, fitness is normalized to the mean fitness of individuals in the parental populations. Simulation parameters: 100 replicates per time point, N = 1000, 20 hybrid incompatibility pairs, s1, s2 and h drawn from distributions (exponential, exponential and uniform, respectively, see details S5 Text).
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Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4359097&req=5

pgen.1005041.g004: Hybrid populations rapidly develop reproductive isolation from both parental species, even in the presence of migration.Once hybrid populations diverge in ancestry at hybrid incompatibility loci from parental populations, individual hybrids have higher fitness on average when they mate with other hybrids in their population compared to either parent. (A) No migration and (B) ongoing migration (4Nm1 = 4Nm2 = 8) from parental populations. Dark points represent the mean fitness, and smears represent the means of 1,000 bootstrap samples. In B, fitness is normalized to the mean fitness of individuals in the parental populations. Simulation parameters: 100 replicates per time point, N = 1000, 20 hybrid incompatibility pairs, s1, s2 and h drawn from distributions (exponential, exponential and uniform, respectively, see details S5 Text).
Mentions: The above simulations focus on simple models that show this process can occur in principle. To capture more biological realism in the number and types of incompatibilities, we simulated 20 incompatibility pairs with randomly determined genomic position and dominance, exponentially distributed selection coefficients (mean s = 0.05) and variation in asymmetry of selection (see above and S5 Text). In these simulations, 95% of populations developed isolation from both parental species. On average, the hybrid population first evolved isolation from both parental species after ~250 generations and was isolated from each by 7 incompatibility pairs within 1000 generations. Since incompatibility pairs with the largest fitness effects tend to fix first, hybrid populations developed considerable reproductive isolation from parental species even before all incompatibilities were fixed in the population (Figs. 4 and S11). Overall, our simulations suggest that rapid evolution of reproductive isolation of hybrid populations is likely when parental species are separated by several hybrid incompatibility pairs.

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