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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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Relationship between the number of hybrid incompatibility pairs and probability of evolving isolation from both parents.With an increasing number of hybrid incompatibility pairs, reproductive isolation from both parents increases in likelihood (A) but populations require longer periods of time to reach parental fitness levels (B). In these simulations two to six hybrid incompatibility pairs distinguish the hybridizing species and hybrid populations formed at equal admixture proportions (f = 0.5, 1,000 diploid individuals). Simulations labeled F1 indicate that the selection coefficients were set such that the fitness of F1 hybrids between the two parental species equaled 0.8 regardless of the number of incompatibilities. Results are based on 500 replicate simulations. In (A) whiskers represent two standard errors; in (B) smears represent the means of 1,000 bootstrap samples.
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pgen.1005041.g003: Relationship between the number of hybrid incompatibility pairs and probability of evolving isolation from both parents.With an increasing number of hybrid incompatibility pairs, reproductive isolation from both parents increases in likelihood (A) but populations require longer periods of time to reach parental fitness levels (B). In these simulations two to six hybrid incompatibility pairs distinguish the hybridizing species and hybrid populations formed at equal admixture proportions (f = 0.5, 1,000 diploid individuals). Simulations labeled F1 indicate that the selection coefficients were set such that the fitness of F1 hybrids between the two parental species equaled 0.8 regardless of the number of incompatibilities. Results are based on 500 replicate simulations. In (A) whiskers represent two standard errors; in (B) smears represent the means of 1,000 bootstrap samples.

Mentions: While selection against hybrids will sometimes be so extreme that few hybrids will survive (or reproduce) in the population (see simulations below), selection against hybrids can also be more moderate, allowing hybrids to persist [41, 45, 49–53]. In simulations of this moderate selection scenario, reproductive isolation between hybrid and parental populations can evolve frequently and rapidly (Fig. 3). For example, for two incompatibility pairs with selection coefficients (s) of 0.1, 47±2% of simulated hybrid populations became isolated from both parental species within an average of ~200 generations. Exploring a range of s (0.1–0.5, S6 Fig., S2 Table), initial admixture proportions (f = 0.3–0.7, S7 Fig.), and population sizes (100–10,000 diploids, S3 Table), we conclude that, unless fitness of hybrids is low (i.e. F1 fitness <0.5) or ancestry of the founding population is substantially skewed (>60% one parental species), reproductive isolation evolves rapidly and with surprisingly high probability (27±2% to 43±2% of the time; on average within 75 ± 16 to 258 ± 38 generations, see S3 Text).


Reproductive isolation of hybrid populations driven by genetic incompatibilities.

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

Relationship between the number of hybrid incompatibility pairs and probability of evolving isolation from both parents.With an increasing number of hybrid incompatibility pairs, reproductive isolation from both parents increases in likelihood (A) but populations require longer periods of time to reach parental fitness levels (B). In these simulations two to six hybrid incompatibility pairs distinguish the hybridizing species and hybrid populations formed at equal admixture proportions (f = 0.5, 1,000 diploid individuals). Simulations labeled F1 indicate that the selection coefficients were set such that the fitness of F1 hybrids between the two parental species equaled 0.8 regardless of the number of incompatibilities. Results are based on 500 replicate simulations. In (A) whiskers represent two standard errors; in (B) smears represent the means of 1,000 bootstrap samples.
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getmorefigures.php?uid=PMC4359097&req=5

pgen.1005041.g003: Relationship between the number of hybrid incompatibility pairs and probability of evolving isolation from both parents.With an increasing number of hybrid incompatibility pairs, reproductive isolation from both parents increases in likelihood (A) but populations require longer periods of time to reach parental fitness levels (B). In these simulations two to six hybrid incompatibility pairs distinguish the hybridizing species and hybrid populations formed at equal admixture proportions (f = 0.5, 1,000 diploid individuals). Simulations labeled F1 indicate that the selection coefficients were set such that the fitness of F1 hybrids between the two parental species equaled 0.8 regardless of the number of incompatibilities. Results are based on 500 replicate simulations. In (A) whiskers represent two standard errors; in (B) smears represent the means of 1,000 bootstrap samples.
Mentions: While selection against hybrids will sometimes be so extreme that few hybrids will survive (or reproduce) in the population (see simulations below), selection against hybrids can also be more moderate, allowing hybrids to persist [41, 45, 49–53]. In simulations of this moderate selection scenario, reproductive isolation between hybrid and parental populations can evolve frequently and rapidly (Fig. 3). For example, for two incompatibility pairs with selection coefficients (s) of 0.1, 47±2% of simulated hybrid populations became isolated from both parental species within an average of ~200 generations. Exploring a range of s (0.1–0.5, S6 Fig., S2 Table), initial admixture proportions (f = 0.3–0.7, S7 Fig.), and population sizes (100–10,000 diploids, S3 Table), we conclude that, unless fitness of hybrids is low (i.e. F1 fitness <0.5) or ancestry of the founding population is substantially skewed (>60% one parental species), reproductive isolation evolves rapidly and with surprisingly high probability (27±2% to 43±2% of the time; on average within 75 ± 16 to 258 ± 38 generations, see S3 Text).

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