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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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Schematic of the simplest “hybrid speciation by genetic incompatibility” scenario.The simplest model hybrid reproductive isolation evolves in a hybrid swarm (S3 Fig.) via fixation of parental genetic incompatibility pairs in opposite directions. Circles indicate the location of incompatibility pairs on chromosomes; yellow shading indicates regions derived from species 1 while blue shading indicates regions derived from species 2. In the first generation, assuming random mating, 50% of individuals will be F1 hybrids if both species contribute equally to the hybrid population. In subsequent generations, recombination will break up ancestry blocks and selection will drive the fixation of parental genotypes at incompatibility loci. In some proportion of cases, incompatibility pairs will fix for opposite parental species genotypes.
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pgen.1005041.g001: Schematic of the simplest “hybrid speciation by genetic incompatibility” scenario.The simplest model hybrid reproductive isolation evolves in a hybrid swarm (S3 Fig.) via fixation of parental genetic incompatibility pairs in opposite directions. Circles indicate the location of incompatibility pairs on chromosomes; yellow shading indicates regions derived from species 1 while blue shading indicates regions derived from species 2. In the first generation, assuming random mating, 50% of individuals will be F1 hybrids if both species contribute equally to the hybrid population. In subsequent generations, recombination will break up ancestry blocks and selection will drive the fixation of parental genotypes at incompatibility loci. In some proportion of cases, incompatibility pairs will fix for opposite parental species genotypes.

Mentions: In its initial description, the BDM model envisioned incompatibilities that cause complete hybrid inviability or sterility, but many negative epistatic interactions in interspecific crosses have more moderate effects on fitness (e.g. [40–42]), allowing hybrid populations to persist. With few exceptions, previous work on genetic incompatibilities has focused on their role in maintaining reproductive isolation between parental species. As a result, hybrid populations have primarily been modeled as tension zones, but incompatibilities may also have interesting dynamics within isolated hybrid populations (i.e. hybrid swarms). Here we present a new model in which reproductive isolation between hybrid and parental populations emerges as a consequence of selection against incompatibilities in a hybrid swarm. Selection on a single adaptive or coevolving incompatibility pair can result in the fixation of genotype combinations that contribute to isolation between the hybrid population and one or the other parental species. Here, we show that in the presence of multiple pairs of such incompatibilities, this process can result in the rapid evolution of reproductive isolation of hybrid populations from both parental species (Fig. 1).


Reproductive isolation of hybrid populations driven by genetic incompatibilities.

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

Schematic of the simplest “hybrid speciation by genetic incompatibility” scenario.The simplest model hybrid reproductive isolation evolves in a hybrid swarm (S3 Fig.) via fixation of parental genetic incompatibility pairs in opposite directions. Circles indicate the location of incompatibility pairs on chromosomes; yellow shading indicates regions derived from species 1 while blue shading indicates regions derived from species 2. In the first generation, assuming random mating, 50% of individuals will be F1 hybrids if both species contribute equally to the hybrid population. In subsequent generations, recombination will break up ancestry blocks and selection will drive the fixation of parental genotypes at incompatibility loci. In some proportion of cases, incompatibility pairs will fix for opposite parental species genotypes.
© Copyright Policy
Related In: Results  -  Collection

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

pgen.1005041.g001: Schematic of the simplest “hybrid speciation by genetic incompatibility” scenario.The simplest model hybrid reproductive isolation evolves in a hybrid swarm (S3 Fig.) via fixation of parental genetic incompatibility pairs in opposite directions. Circles indicate the location of incompatibility pairs on chromosomes; yellow shading indicates regions derived from species 1 while blue shading indicates regions derived from species 2. In the first generation, assuming random mating, 50% of individuals will be F1 hybrids if both species contribute equally to the hybrid population. In subsequent generations, recombination will break up ancestry blocks and selection will drive the fixation of parental genotypes at incompatibility loci. In some proportion of cases, incompatibility pairs will fix for opposite parental species genotypes.
Mentions: In its initial description, the BDM model envisioned incompatibilities that cause complete hybrid inviability or sterility, but many negative epistatic interactions in interspecific crosses have more moderate effects on fitness (e.g. [40–42]), allowing hybrid populations to persist. With few exceptions, previous work on genetic incompatibilities has focused on their role in maintaining reproductive isolation between parental species. As a result, hybrid populations have primarily been modeled as tension zones, but incompatibilities may also have interesting dynamics within isolated hybrid populations (i.e. hybrid swarms). Here we present a new model in which reproductive isolation between hybrid and parental populations emerges as a consequence of selection against incompatibilities in a hybrid swarm. Selection on a single adaptive or coevolving incompatibility pair can result in the fixation of genotype combinations that contribute to isolation between the hybrid population and one or the other parental species. Here, we show that in the presence of multiple pairs of such incompatibilities, this process can result in the rapid evolution of reproductive isolation of hybrid populations from both parental species (Fig. 1).

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