A Note on Haldane's Rule: Hybrid Inviability Versus Hybrid Sterility

Evolution ◽  
1992 ◽  
Vol 46 (5) ◽  
pp. 1584 ◽  
Author(s):  
Chung-I Wu
Keyword(s):  
Hybrid Sterility ◽  
Hybrid Inviability ◽  
Haldane’S Rule ◽  
Haldane's Rule

scholarly journals A NOTE ON HALDANE'S RULE: HYBRID INVIABILITY VERSUS HYBRID STERILITY

Evolution ◽  
1992 ◽  
Vol 46 (5) ◽  
pp. 1584-1587 ◽  
Author(s):  
Chung-I Wu
Keyword(s):  
Hybrid Sterility ◽  
Hybrid Inviability ◽  
Haldane’S Rule ◽  
Haldane's Rule

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 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 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.

scholarly journals Complex basis of hybrid female sterility and Haldane's rule in Heliconius butterflies: Z-linkage and epistasis

2021 ◽  
Author(s):  
Neil Rosser ◽  
Nathaniel B. Edelman ◽  
Lucie Queste ◽  
Michaela Nelson ◽  
Fernando A. Seixas ◽  
...  
Keyword(s):  
Sex Chromosome ◽  
Hybrid Sterility ◽  
Differentially Expressed ◽  
F1 Hybrids ◽  
Female Sterility ◽  
Ovary Development ◽  
Z Chromosome ◽  
Hybrid Female ◽  
Haldane’S Rule ◽  
Haldane's Rule

Hybrids between diverging populations are often sterile or inviable. Hybrid unfitness usually evolves first in the heterogametic sex -- a pattern known as Haldane's rule. The genetics of Haldane's Rule have been extensively studied in species where the male is the heterogametic (XX/XY) sex, but its basis in taxa where the female is heterogametic (ZW/ZZ), such as Lepidoptera and birds, is largely unknown. Here, we analyse a new case of female hybrid sterility between geographic subspecies of Heliconius pardalinus. The two subspecies mate freely in captivity, but female F1 hybrids in both directions of cross are sterile. Sterility is due to arrested development of oocytes after they become differentiated from nurse cells, but before yolk deposition. We backcrossed fertile male F1 hybrids to parental females, and mapped quantitative trait loci (QTLs) for female sterility. We also identified genes differentially expressed in the ovary, and as a function of oocyte development. The Z chromosome has a major effect, similar to the "large X effect" in Drosophila, with strong epistatic interactions between loci at either end of the Z chromosome, and between the Z chromosome and autosomal loci on chromosomes 8 and 20. Among loci differentially expressed between females with arrested vs. non-arrested ovary development, we identified six candidate genes known also from Drosophila melanogaster and Parage aegeria oogenesis. This study is the first to characterize hybrid sterility using genome mapping in the Lepidoptera. We demonstrate that sterility is produced by multiple complex epistastic interactions often involving the sex chromosome, as predicted by the dominance theory of Haldane's Rule.

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 Speciation by Reinforcement: A Model Derived from Studies of Drosophila

Genetics ◽  
1996 ◽  
Vol 143 (3) ◽  
pp. 1485-1497 ◽  
Author(s):  
John K Kelly ◽  
Mohamed A F Noor
Keyword(s):  
Hybrid Sterility ◽  
Hybrid Fitness ◽  
Genetic Studies ◽  
Haldane’S Rule ◽  
Female Mating ◽  
Haldane's Rule ◽  
Male Characters ◽  
Fertility Reduction ◽  
Female Mating Preferences ◽  
Viable Mechanism

Abstract Reinforcement is an increase in premating reproductive isolation between taxa resulting from selection against hybrids. We present a model of reinforcement with a novel type of selection on female mating behavior. Previous models of reinforcement have focused on the divergence of female mating preferences between nascent species. We suggest that an increase in the level of female mating discrimination can yield reinforcement without further divergence of either male characters or female preferences. This model indicates that selection on mating discrimination is a viable mechanism for reinforcement and may allow speciation under less stringent conditions than selection on female preference. This model also incorporates empirical results from genetic studies of hybrid fitness determination in Drosophila species. We find that the details of inheritance, which include sex-linked transmission, sex-limited fertility reduction, and X-autosome epistasis, have important effects on the likelihood of reinforcement. In particular, X-autosome epistasis for hybrid fitness determination facilitates reinforcement when hybrid fertility reduction occurs in males, but hinders the process when it occurs in females. Haldane's rule indicates that hybrid sterility will generally evolve in males prior to females within nascent species. Thus, Haldane's rule and X-autosome epistasis provide conditions that are surprisingly favorable for reinforcement in Drosophila.

scholarly journals Hybrid Sterility, Haldane's Rule and Speciation in Heliconius cydno and H. melpomene

Genetics ◽  
2002 ◽  
Vol 161 (4) ◽  
pp. 1517-1526 ◽  
Author(s):  
Russell E Naisbit ◽  
Chris D Jiggins ◽  
Mauricio Linares ◽  
Camilo Salazar ◽  
James Mallet
Keyword(s):  
Hybrid Sterility ◽  
Female Offspring ◽  
F1 Hybrids ◽  
Female Sterility ◽  
Haldane’S Rule ◽  
Haldane's Rule ◽  
In The Wild ◽  
Multiple Routes ◽  
Female Hybrid ◽  
Heterogametic Sex

Abstract Most genetic studies of Haldane's rule, in which hybrid sterility or inviability affects the heterogametic sex preferentially, have focused on Drosophila. It therefore remains unclear to what extent the conclusions of that work apply more generally, particularly in female-heterogametic taxa such as birds and Lepidoptera. Here we present a genetic analysis of Haldane's rule in Heliconius butterflies. Female F1 hybrids between Heliconius melpomene and H. cydno are completely sterile, while males have normal to mildly reduced fertility. In backcrosses of male F1 hybrids, female offspring range from completely sterile to fully fertile. Linkage analysis using the Z-linked triose-phosphate isomerase locus demonstrates a “large X” (Z) effect on sterility. Expression of female sterility varies among crosses in this and a previous study of Heliconius. Sterility may result from the production of normal but infertile eggs, production of small infertile eggs, or from a complete failure to develop ovarioles, which suggests multiple routes to the evolution of hybrid sterility in these Heliconius species. These results conform to the expectations of the “dominance” rather than “faster male” theories of Haldane's rule and suggest that relatively few loci are responsible. The two species are broadly sympatric and hybridize in the wild, so that female hybrid sterility forms one of several strong but incomplete barriers to gene flow in nature. The effect of female sterility is comparable to that of selection against non-mimetic hybrids, while mate choice forms a much stronger barrier to gene transfer.

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