scholarly journals A rare exception to Haldane’s rule: Are X chromosomes key to hybrid incompatibilities?

Heredity ◽  
2017 ◽  
Vol 118 (6) ◽  
pp. 554-562 ◽  
Author(s):  
P A Moran ◽  
M G Ritchie ◽  
N W Bailey
Genetics ◽  
1995 ◽  
Vol 140 (1) ◽  
pp. 389-402 ◽  
Author(s):  
M Turelli ◽  
H A Orr

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.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Terence J. Robinson ◽  
Halina Cernohorska ◽  
Svatava Kubickova ◽  
Miluse Vozdova ◽  
Petra Musilova ◽  
...  

AbstractChromosome structural change has long been considered important in the evolution of post-zygotic reproductive isolation. The premise that karyotypic variation can serve as a possible barrier to gene flow is founded on the expectation that heterozygotes for structurally distinct chromosomal forms would be partially sterile (negatively heterotic) or show reduced recombination. We report the outcome of a detailed comparative molecular cytogenetic study of three antelope species, genus Raphicerus, that have undergone a rapid radiation. The species are largely conserved with respect to their euchromatic regions but the X chromosomes, in marked contrast, show distinct patterns of heterochromatic amplification and localization of repeats that have occurred independently in each lineage. We argue a novel hypothesis that postulates that the expansion of heterochromatic blocks in the homogametic sex can, with certain conditions, contribute to post-zygotic isolation. i.e., female hybrid incompatibility, the converse of Haldane’s rule. This is based on the expectation that hybrids incur a selective disadvantage due to impaired meiosis resulting from the meiotic checkpoint network’s surveillance of the asymmetric expansions of heterochromatic blocks in the homogametic sex. Asynapsis of these heterochromatic regions would result in meiotic silencing of unsynapsed chromatin and, if this persists, germline apoptosis and female infertility.


Genetics ◽  
2000 ◽  
Vol 154 (4) ◽  
pp. 1663-1679 ◽  
Author(s):  
Michael Turelli ◽  
H Allen Orr

Abstract The sterility and inviability of species hybrids can be explained by between-locus “Dobzhansky-Muller” incompatibilities: alleles that are fit on their “normal” genetic backgrounds sometimes lower fitness when brought together in hybrids. We present a model of two-locus incompatibilities that distinguishes among three types of hybrid interactions: those between heterozygous loci (H0), those between a heterozygous and a homozygous (or hemizygous) locus (H1), and those between homozygous loci (H2). We predict the relative fitnesses of hybrid genotypes by calculating the expected numbers of each type of incompatibility. We use this model to study Haldane's rule and the large effect of X chromosomes on postzygotic isolation. We show that the severity of H0 vs. H1 incompatibilities is key to understanding Haldane's rule, while the severity of H1 vs. H2 incompatibilities must also be considered to explain large X effects. Large X effects are not inevitable in backcross analyses but rather—like Haldane's rule—may often reflect the recessivity of alleles causing postzygotic isolation. We also consider incompatibilities involving the Y (or W) chromosome and maternal effects. Such incompatibilities are common in Drosophila species crosses, and their consequences in male- vs. female-heterogametic taxa may explain the pattern of exceptions to Haldane's rule.


Genetics ◽  
1997 ◽  
Vol 147 (4) ◽  
pp. 1799-1815 ◽  
Author(s):  
Michael Turelli ◽  
David J Begun

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.


Genetics ◽  
1996 ◽  
Vol 143 (1) ◽  
pp. 603-607
Author(s):  
Ling-Wen Zeng

Evolution ◽  
2005 ◽  
Vol 59 (5) ◽  
pp. 1016-1026 ◽  
Author(s):  
Michel Slotman ◽  
Alessandra Della Torre ◽  
Jeffrey R. Powell

2013 ◽  
Vol 9 (5) ◽  
pp. 20130327 ◽  
Author(s):  
Matthew Schrader ◽  
Rebecca C. Fuller ◽  
Joseph Travis

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.


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