Bounds to parapatric speciation: A Dobzhansky-Muller incompatibility model involving autosomes, X chromosomes, and mitochondria

Höllinger, Ilse; Hermisson, Joachim

doi:10.1111/evo.13223

Cited by 25 publications

(23 citation statements)

References 83 publications

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“…when the neutral marker is close to a multilocus barrier). This result mirrors earlier predictions for single and two-locus barriers under a regime where introgressed alleles are rare (Muirhead and Presgraves, 2016); and for the maintenance of DMIs in parapatry (Hoellinger and Hermisson, 2017). Albeit it is a moderate effect, this process is very general as it applies to species diverging in parapatry under various scenarios (including dosage compensation, sex-biased migration and sex-biased selection).…”

Section: Discussionsupporting

confidence: 88%

“…Moreover, the greatest sex chromosome-to-autosome difference in barrier strength occurs when incompatible alleles are recessive and dosage compensated in the heterogametic sex (in agreement with Muirhead and Presgraves (2016); and Hoellinger and Hermisson (2017) who assume recessivity of the DMI itself). Importantly under our model assumptions, dominance (i.e.…”

Section: Discussionmentioning

confidence: 82%

“…In a model of parapatry, Hoellinger and Hermisson (2017) found that pairs of sex-linked DMIs are more easily maintained in the presence of interspecies gene flow than autosomal DMIs, especially in the presence of dosage compensation and/or male-biased migration. However, these studies do not explicitly quantify the long-term effect of interspecies barriers on neutral gene flow, and they are limited to the special case of pairs of DMIs.…”

Section: Introductionmentioning

confidence: 99%

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The rates of introgression and barriers to genetic exchange between hybridizing species: sex chromosomes vs. autosomes

Fraïssé

Sachdeva

2020

Preprint

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Interspecific crossing experiments have shown that sex chromosomes play a major role in the reproductive isolation of many species. However, their ability to act as reproductive barriers, which hamper interspecific genetic exchange, has hardly been evaluated quantitatively in relation to autosomes. Yet, this genome-wide limitation of gene flow is essential for understanding the complete separation of species, and thus speciation. Here, we develop a mainland-island model of secondary contact between hybridizing species of a XY (or ZW) sexual system. We obtain theoretical predictions for the frequency of introgressed alleles, and the strength of the barrier to neutral gene flow of the two types of chromosomes carrying multiple interspecific barrier loci. Theoretical predictions are obtained for scenarios where introgressed alleles are rare. We show that the same analytical expressions apply for sex chromosomes and autosomes, but with different effective parameters. The specific features of sex chromosomes (hemizygosity and absence of recombination in the heterogametic sex) lead to reduced levels of introgression of the X (or Z) compared to autosomes. This effect is enhanced by certain types of dosage compensation or sex-biased forces; but it remains overall small (except when incompatibilities are recessive). We discuss these predictions in light of empirical data comprising model-based tests of introgression and dine surveys in various biological systems.

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Section: Discussionsupporting

confidence: 88%

Section: Discussionmentioning

confidence: 82%

Section: Introductionmentioning

confidence: 99%

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The rates of introgression and barriers to genetic exchange between hybridizing species: sex chromosomes vs. autosomes

Fraïssé

Sachdeva

2020

Preprint

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“…The Bateson-Dobzhansky-Muller model (Bateson, 1909;Dobzhansky, 1936;Muller, 1942) characterizes the emergence of incompatibilities between two allopatric populations due to the fixation of variants within one population that, while neutral in their original background, are deleterious in the genetic background of the other. Burton and Barreto (2012) highlight numerous such incompatibilities between mitochondrial and nuclear genomes that result in hybrid breakdown, and the evolution of pairwise incompatibilities among mitochondrial, autosomal, and X-linked genes in parapatric populations has also been further explored through analytical models (Höllinger and Hermisson, 2017) . While our models only consider a single population, the potential rapid fixation of both alleles in every model highlights the potential accumulation of two variants that in combination are either neutral or advantageous.…”

Section: Discussionmentioning

confidence: 99%

Sexual Conflict through Mother’s Curse and Father’s Curse

Ågren

Munasinghe

Clark

2018

Preprint

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In contrast with autosomes, lineages of sex chromosomes reside for different amounts of time in males and females, and this transmission asymmetry makes them hotspots for sexual conflict. Similarly, the maternal inheritance of the mitochondrial genome (mtDNA) means that mutations that are beneficial in females can spread in a population even if they are deleterious in males, a form of sexual conflict known as Mother's Curse. While both Mother's Curse and sex chromosome induced sexual conflict have been well studied on their own, the interaction between mitochondrial genes and genes on sex chromosomes is poorly understood. Here, we use analytical models and computer simulations to perform a comprehensive examination of how transmission asymmetries of nuclear, mitochondrial, and sex chromosome-linked genes may both cause and resolve sexual conflicts. For example, the accumulation of male-biased Mother's Curse mtDNA mutations will lead to selection in males for compensatory nuclear modifier loci that alleviate the effect. We show how the Y chromosome, being strictly paternally transmitted provides a particularly safe harbor for such modifiers. This analytical framework also allows us to discover a novel kind of sexual conflict, by which Y chromosome-autosome epistasis may result in the spread of male beneficial but female deleterious mutations in a population. We christen this phenomenon Father's Curse. Extending this analytical framework to ZW sex chromosome systems, where males are the heterogametic sex, we also show how W-autosome epistasis can lead to a novel kind of nuclear Mother's Curse. Overall, this study provides a comprehensive framework to understand how genetic transmission asymmetries may both cause and resolve sexual conflicts.

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“…This is expected to lead to faster evolution in the sex chromosomes (Charlesworth, Coyne, & Barton, 1987) that may partly underlie the large-X effect (Presgraves, 2008). The large-X effect refers to the observation that the sex chromosomes seem to play a special role in speciation by acting as the strongest barrier for gene flow between hybridizing lineages across different species (H€ ollinger & Hermisson, 2017). Similarly, haplodiploid species have been suggested to acquire reproductive isolation earlier and speciate faster than diploid species (Lima, 2014;Lohse & Ross, 2015).…”

mentioning

confidence: 99%

Conflict between heterozygote advantage and hybrid incompatibility in haplodiploids (and sex chromosomes)

et al. 2018

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In many diploid species, the sex chromosomes play a special role in mediating reproductive isolation. In haplodiploids, where females are diploid and males haploid, the whole genome behaves similarly to the X/Z chromosomes of diploids. Therefore, haplodiploid systems can serve as a model for the role of sex chromosomes in speciation and hybridization. A previously described population of Finnish Formica wood ants displays genome-wide signs of ploidally and sexually antagonistic selection resulting from hybridization. Here, hybrid females have increased survivorship but hybrid males are inviable. To understand how the unusual hybrid population may be maintained, we developed a mathematical model with hybrid incompatibility, female heterozygote advantage, recombination and assortative mating. The rugged fitness landscape resulting from the co-occurrence of heterozygote advantage and hybrid incompatibility results in a sexual conflict in haplodiploids, which is caused by the ploidy difference. Thus, whereas heterozygote advantage always promotes long-term polymorphism in diploids, we find various outcomes in haplodiploids in which the population stabilizes either in favour of males, females or via maximizing the number of introgressed individuals. We discuss these outcomes with respect to the potential long-term fate of the Finnish wood ant population and provide approximations for the extension of the model to multiple incompatibilities. Moreover, we highlight the general implications of our results for speciation and hybridization in haplodiploids versus diploids and how the described fitness relationships could contribute to the outstanding role of sex chromosomes as hotspots of sexual antagonism and genes involved in speciation.

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Bounds to parapatric speciation: A Dobzhansky-Muller incompatibility model involving autosomes, X chromosomes, and mitochondria

Cited by 25 publications

References 83 publications

The rates of introgression and barriers to genetic exchange between hybridizing species: sex chromosomes vs. autosomes

The rates of introgression and barriers to genetic exchange between hybridizing species: sex chromosomes vs. autosomes

Sexual Conflict through Mother’s Curse and Father’s Curse

Conflict between heterozygote advantage and hybrid incompatibility in haplodiploids (and sex chromosomes)

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