scholarly journals Haldane’s rule in the placenta: sex-biased misregulation of the Kcnq1 imprinting cluster in hybrid mice

2020 ◽  
Author(s):  
Lena Arévalo ◽  
Sarah Gardner ◽  
Polly Campbell
Keyword(s):  
X Chromosome ◽  
Imprinted Genes ◽  
Mus Musculus Domesticus ◽  
Hybrid Inviability ◽  
Biallelic Expression ◽  
Haldane’S Rule ◽  
Haldane's Rule ◽  
Parent Of Origin ◽  
Strong Candidate ◽  
Growth Abnormalities

ABSTRACTMammalian hybrids often show striking asymmetries in their phenotypes both between reciprocal crosses, and between sexes in accordance with Haldane’s rule. Hybrid inviability is associated with parent-of-origin placental growth abnormalities for which misregulation of imprinted genes is a strong candidate mechanism. However, direct evidence for the involvement of abnormal imprinting and the mechanisms behind this proposed misregulation is limited. We used transcriptome and reduced representation bisulfite sequencing to evaluate the contribution of imprinted genes to a long-standing example of parent-of-origin placental growth dysplasia in the cross between the house mouse (Mus musculus domesticus) and the Algerian mouse (Mus spretus). We found little evidence for loss of imprinting and imprinted genes with biallelic expression were not misexpressed. Instead, imprinted genes with transgressive expression and methylation were concentrated in the Kcnq1 cluster, which contains causal genes for prenatal growth abnormalities in both mice and humans. Hypermethylation of the cluster’s imprinting control region, and consequent misexpression of the genes Phlda2 and Ascl2, is a strong candidate mechanism for hybrid placental undergrowth. Transgressive placental and gene regulatory phenotypes, including expression and methylation in the Kcnq1 cluster, were more extreme in hybrid males. While consistent with Haldane’s rule, male-biased defects are not expected in rodent placenta because the maternal X chromosome is effectively hemizygous in both sexes. In search of an explanation we found evidence of leaky imprinted X-chromosome inactivation in hybrid females. Supplementary expression from the paternal X-chromosome may buffer the females from the effects of X-linked incompatibilities to which males are fully exposed. Sex differences in chromatin structure on the X and sex-biased maternal effects are non-mutually exclusive alternative explanations for adherence to Haldane’s rule in hybrid placenta. The results of this study contribute to understanding of the genetic basis of hybrid inviability in mammals, and the role of imprinted genes in speciation.

scholarly journals Differences in offspring size predict the direction of isolation asymmetry between populations of a placental fish

2013 ◽  
Vol 9 (5) ◽  
pp. 20130327 ◽  
Author(s):  
Matthew Schrader ◽  
Rebecca C. Fuller ◽  
Joseph Travis
Keyword(s):  
Reproductive Isolation ◽  
Offspring Size ◽  
Hybrid Inviability ◽  
Haldane’S Rule ◽  
Haldane's Rule ◽  
Asymmetric Pattern ◽  
Heterandria Formosa ◽  
Different Populations ◽  
Selection For

Crosses between populations or species often display an asymmetry in the fitness of reciprocal F 1 hybrids. This pattern, referred to as isolation asymmetry or Darwin's Corollary to Haldane's Rule, has been observed in taxa from plants to vertebrates, yet we still know little about which factors determine its magnitude and direction. Here, we show that differences in offspring size predict the direction of isolation asymmetry observed in crosses between populations of a placental fish, Heterandria formosa . In crosses between populations with differences in offspring size, high rates of hybrid inviability occur only when the mother is from a population characterized by small offspring. Crosses between populations that display similarly sized offspring, whether large or small, do not result in high levels of hybrid inviability in either direction. We suggest this asymmetric pattern of reproductive isolation is due to a disruption of parent–offspring coadaptation that emerges from selection for differently sized offspring in different populations.

scholarly journals Restricted X chromosome introgression and support for Haldane's rule in hybridizing damselflies

2021 ◽  
Author(s):  
Janne Swaegers ◽  
Rosa Ana Sanchez-Guillen ◽  
Pallavi Chauhan ◽  
Maren Wellenreuther ◽  
Bengt Hansson
Keyword(s):  
X Chromosome ◽  
Sex Chromosomes ◽  
Hybrid Zones ◽  
Haldane’S Rule ◽  
Haldane's Rule ◽  
Genome Wide ◽  
Determination System ◽  
Heterogametic Sex ◽  
Sex Determination System ◽  
Genomic Introgression

Contemporary hybrid zones act as natural laboratories for the investigation of species boundaries and allow to shed light on the little understood roles of sex chromosomes in species divergence. Sex chromosomes are considered to function as a hotspot of genetic divergence between species; indicated by less genomic introgression compared to autosomes during hybridisation. Moreover, they are thought to contribute to Haldane's rule which states that hybrids of the heterogametic sex are more likely to be inviable or sterile. To test these hypotheses, we used contemporary hybrid zones of Ischnura elegans, a damselfly species that has been expanding its range into the northern and western regions of Spain, leading to chronic hybridization with its sister species Ischnura graellsii. We analysed genome-wide SNPs in the Spanish I. elegans and I. graellsii hybrid zone and found (i) that the X chromosome shows less genomic introgression compared to autosomes and (ii) that males are underrepresented among admixed individuals as predicted by Haldane's rule. This is the first study in Odonata that suggests a role of the X chromosome in reproductive isolation. Moreover, our data adds to the few studies on species with X0 sex determination system and contradicts the hypothesis that the absence of a Y chromosome causes exceptions to Haldane's rule.

scholarly journals The dominance theory of Haldane's rule.

Genetics ◽  
1995 ◽  
Vol 140 (1) ◽  
pp. 389-402 ◽  
Author(s):  
M Turelli ◽  
H A Orr
Keyword(s):  
Cumulative Effects ◽  
Postzygotic Isolation ◽  
Hybrid Fitness ◽  
Hybrid Inviability ◽  
X Chromosomes ◽  
F1 Hybrid ◽  
Haldane’S Rule ◽  
Simple Hypothesis ◽  
Haldane's Rule ◽  
Species Hybrids

Abstract "HALDANE's rule" states that, if species hybrids of one sex only are inviable or sterile, the afflicted sex is much more likely to be heterogametic (XY) than homogametic (XX). We show that most or all of the phenomena associated with HALDANE's rule can be explained by the simple hypothesis that alleles decreasing hybrid fitness are partially recessive. Under this hypothesis, the XY sex suffers more than the XX because X-linked alleles causing postzygotic isolation tend to have greater cumulative effects when hemizygous than when heterozygous, even though the XX sex carries twice as many such alleles. The dominance hypothesis can also account for the "large X effect," the disproportionate effect of the X chromosome on hybrid inviability/sterility. In addition, the dominance theory is consistent with: the long temporal lag between the evolution of heterogametic and homogametic postzygotic isolation, the frequency of exceptions to HALDANE's rule, puzzling Drosophila experiments in which "unbalanced" hybrid females, who carry two X chromosomes from the same species, remain fertile whereas F1 hybrid males are sterile, and the absence of cases of HALDANE's rule for hybrid inviability in mammals. We discuss several novel predictions that could lead to rejection of the dominance theory.

SEX CHROMOSOME TRANSLOCATIONS IN THE EVOLUTION OF REPRODUCTIVE ISOLATION

Genetics ◽  
1972 ◽  
Vol 72 (2) ◽  
pp. 317-333
Author(s):  
Martin L Tracey
Keyword(s):  
Reproductive Isolation ◽  
X Chromosome ◽  
Sex Chromosome ◽  
Hybrid Sterility ◽  
Fixation Probability ◽  
Chromosomal Imbalance ◽  
Haldane’S Rule ◽  
Chromosome Translocations ◽  
Haldane's Rule ◽  
Heterogametic Sex

ABSTRACT Haldane's rule states that in organisms with differentiated sex chromosomes, hybrid sterility or inviability is generally expressed more frequently in the heterogametic sex. This observation has been variously explained as due to either genic or chromosomal imbalance. The fixation probabilities and mean times to fixation of sex-chromosome translocations of the type necessary to explain Haldane's rule on the basis of chromosomal imbalance have been estimated in small populations of Drosophila melanogaster. The fixation probability of an X chromosome carrying the long arm of the Y(X.YL) is approximately 30% greater than expected under the assumption of no selection. No fitness differences associated with the attached YL segment were detected. The fixation probability of a deficient Y chromosome is 300% greater than expected when the X chromosome contains the deleted portion of the Y. It is suggested that sex-chromosome translocations may play a role in the establishment of reproductive isolation.

scholarly journals Haldane's Rule and X-chromosome Size in Drosophila

Genetics ◽  
1997 ◽  
Vol 147 (4) ◽  
pp. 1799-1815 ◽  
Author(s):  
Michael Turelli ◽  
David J Begun
Keyword(s):  
X Chromosome ◽  
Divergence Time ◽  
Nuclear Genome ◽  
Similar Rate ◽  
Heterogeneous Data ◽  
Genetic Distances ◽  
X Chromosomes ◽  
Haldane’S Rule ◽  
Haldane's Rule ◽  
Heterogametic Sex

Abstract The “dominance theory” of Haldane's rule postulates that hybrids of the heterogametic sex are more likely to be inviable or sterile than the homogametic sex because some of the epistatic incompatibilities contributing to postzygotic isolation behave as X-linked partial recessives. When this is true, pairs of taxa with relatively large X chromosomes should require less divergence time, on average, to produce Haldane's rule than pairs with smaller Xs. Similarly, if the dominance theory is correct and if the X chromosome evolves at a similar rate to the autosomes, the size of the X should not influence the rate at which homogametic hybrids become inviable or sterile. We use Drosophila data to examine both of these predictions. As expected under the dominance theory, pairs of taxa with large X chromosomes (~40% of the nuclear genome) show Haldane's rule for sterility at significantly smaller genetic distances than pairs with smaller X chromosomes (~20% of the genome). As also predicted, the genetic distances between taxa that exhibit female inviability/sterility show no differences between “large X” vs. “small X” pairs. We present some simple mathematical models to relate these data to the dominance theory and alternative hypotheses involving faster evolution of the X vs. the autosomes and/or faster evolution of incompatibilities that produce male-specific vs. female-specific sterility. Although the data agree qualitatively with the predictions of the dominance theory, they depart significantly from the quantitative predictions of simple models of the dominance theory and the other hypotheses considered. These departures probably stem from the many simplifying assumptions needed to tractably model epistatic incompatibilities and to analyze heterogeneous data from many taxa.

scholarly journals Genomic imprinting in mouse blastocysts is predominantly associated with H3K27me3

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Laura Santini ◽  
Florian Halbritter ◽  
Fabian Titz-Teixeira ◽  
Toru Suzuki ◽  
Maki Asami ◽  
...  
Keyword(s):  
Bisulfite Sequencing ◽  
Blastocyst Stage ◽  
Preimplantation Embryos ◽  
Imprinted Genes ◽  
Specific Expression ◽  
Histone 3 ◽  
Complex Program ◽  
Genome Bisulfite Sequencing ◽  
Mammalian Genomes ◽  
Parent Of Origin

AbstractIn mammalian genomes, differentially methylated regions (DMRs) and histone marks including trimethylation of histone 3 lysine 27 (H3K27me3) at imprinted genes are asymmetrically inherited to control parentally-biased gene expression. However, neither parent-of-origin-specific transcription nor imprints have been comprehensively mapped at the blastocyst stage of preimplantation development. Here, we address this by integrating transcriptomic and epigenomic approaches in mouse preimplantation embryos. We find that seventy-one genes exhibit previously unreported parent-of-origin-specific expression in blastocysts (nBiX: novel blastocyst-imprinted expressed). Uniparental expression of nBiX genes disappears soon after implantation. Micro-whole-genome bisulfite sequencing (µWGBS) of individual uniparental blastocysts detects 859 DMRs. We further find that 16% of nBiX genes are associated with a DMR, whereas most are associated with parentally-biased H3K27me3, suggesting a role for Polycomb-mediated imprinting in blastocysts. nBiX genes are clustered: five clusters contained at least one published imprinted gene, and five clusters exclusively contained nBiX genes. These data suggest that early development undergoes a complex program of stage-specific imprinting involving different tiers of regulation.

scholarly journals Resurrecting Muller's Theory of Haldane's Rule

Genetics ◽  
1996 ◽  
Vol 143 (1) ◽  
pp. 603-607
Author(s):  
Ling-Wen Zeng
Keyword(s):  
Haldane’S Rule ◽  
Haldane's Rule
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