Chromosomal evolution in Raphicerus antelope suggests divergent X chromosomes may drive speciation through females, rather than males, contrary to Haldane's rule

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.

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The dominance theory of Haldane's rule.

Genetics ◽

10.1093/genetics/140.1.389 ◽

1995 ◽

Vol 140 (1) ◽

pp. 389-402 ◽

Cited By ~ 17

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.

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Analysis of autosomal polygenic variation for the expression of Haldane's rule in flour beetles.

Genetics ◽

10.1093/genetics/138.3.791 ◽

1994 ◽

Vol 138 (3) ◽

pp. 791-799

Author(s):

M J Wade ◽

N A Johnson ◽

G Wardle

Keyword(s):

Genetic Basis ◽

Interspecific Crosses ◽

Heritable Variation ◽

Hybrid Male ◽

Hybrid Incompatibility ◽

Haldane’S Rule ◽

Haldane's Rule ◽

Flour Beetles ◽

Heterogametic Sex ◽

Polygenic Variation

Abstract Haldane's rule states that, in interspecific crosses, when hybrid viability or fertility is diminished more in one sex of the hybrids than in the other, the heterogametic sex is more adversely affected. We used quantitative genetic methods to investigate the genetic basis of variation for the expression of the viability aspect of Haldane's rule when Tribolium castaneum males are crossed to Tribolium freemani females. Using a half-sib design, we found significant genetic variance for the expression of Haldane's rule, i.e., variation among T. castaneum sires in the hybrid sex ratios produced by their sons. We also derived 23 independent lineages from the same base population by 8 generations of brother-sister mating. From the same experiments, we also found heritable variation among surviving hybrid males in the incidence of antennal deformities. Upon inbreeding, the variance of both traits (hybrid sex ratio and proportion deformities) increased substantially but the means changed little. Because fitness within T. castaneum lineages declined substantially with inbreeding, we infer that hybrid male viability may have a different genetic basis than viability fitness within species. Deleterious recessive alleles held within species by mutation/selection balance appear not to be a major contributor to hybrid incompatibility.

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Dominance, Epistasis and the Genetics of Postzygotic Isolation

Genetics ◽

10.1093/genetics/154.4.1663 ◽

2000 ◽

Vol 154 (4) ◽

pp. 1663-1679 ◽

Cited By ~ 6

Author(s):

Michael Turelli ◽

H Allen Orr

Keyword(s):

Maternal Effects ◽

Drosophila Species ◽

W Chromosome ◽

Postzygotic Isolation ◽

X Chromosomes ◽

Haldane’S Rule ◽

Haldane's Rule ◽

Species Hybrids

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.

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

Heredity ◽

10.1038/hdy.2016.127 ◽

2017 ◽

Vol 118 (6) ◽

pp. 554-562 ◽

Cited By ~ 6

Author(s):

P A Moran ◽

M G Ritchie ◽

N W Bailey

Keyword(s):

X Chromosomes ◽

Haldane’S Rule ◽

Haldane's Rule ◽

Rare Exception

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Haldane's Rule and X-chromosome Size in Drosophila

Genetics ◽

10.1093/genetics/147.4.1799 ◽

1997 ◽

Vol 147 (4) ◽

pp. 1799-1815 ◽

Cited By ~ 3

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.

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

Genetics ◽

10.1093/genetics/161.4.1517 ◽

2002 ◽

Vol 161 (4) ◽

pp. 1517-1526 ◽

Cited By ~ 2

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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