The genetic basis of Haldane's rule and the nature of asymmetric hybrid male sterility among Drosophila simulans, Drosophila mauritiana and Drosophila sechellia.

Abstract Haldane's rule (i.e., the preferential hybrid sterility and inviability of heterogametic sex) has been known for 70 years, but its genetic basis, which is crucial to the understanding of the process of species formation, remains unclear. In the present study, we have investigated the genetic basis of hybrid male sterility using Drosophila simulans, Drosophila mauritiana and Drosophila sechellia. An introgression of D. sechellia Y chromosome into a fairly homogenous background of D. simulans did not show any effect of the introgressed Y on male sterility. The substitution of D. simulans Y chromosome into D. sechellia, and both reciprocal Y chromosome substitutions between D. simulans and D. mauritiana were unsuccessful. Introgressions of cytoplasm between D. simulans and D. mauritiana (or D. sechellia) also did not have any effect on hybrid male sterility. These results rule out the X-Y interaction hypothesis as a general explanation of Haldane's rule in this species group and indicate an involvement of an X-autosome interaction. Models of symmetrical and asymmetrical X-autosome interaction have been developed which explain the Y chromosome substitution results and suggest that evolution of interactions between different genetic elements in the early stages of speciation is more likely to be of an asymmetrical nature. The model of asymmetrical X-autosome interaction also predicts that different sets of interacting genes may be involved in different pairs of related species and can account for the observation that hybrid male sterility in many partially isolated species is often nonreciprocal or unidirectional.

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Extensive introgression despite Haldane’s rule: insights from grasshopper hybrid zones

10.22541/au.163785413.32517525/v1 ◽

2021 ◽

Author(s):

Linda Hagberg ◽

Enrique Celemin ◽

Iker Irisarri ◽

Oliver Hawlitschek ◽

J L Bella ◽

...

Keyword(s):

Gene Flow ◽

Reproductive Isolation ◽

Male Sterility ◽

Secondary Contact ◽

Hybrid Zones ◽

Hybrid Male ◽

Hybrid Male Sterility ◽

Haldane’S Rule ◽

Haldane's Rule ◽

Species Formation

Although the process of species formation is notoriously idiosyncratic, the observation of pervasive patterns of reproductive isolation across species pairs suggests that generalities, or “rules”, underlie species formation in all animals. Haldane’s rule states that whenever a sex is absent, rare or sterile in a cross between two taxa, that sex is usually the heterogametic sex. Yet, understanding how Haldane’s rule first evolves and whether it is associated to genome wide barriers to gene flow remains a challenging task because this rule is usually studied in highly divergent taxa that no longer hybridize in nature. Here, we address these questions using the meadow grasshopper Pseudochorthippus parallelus where populations that readily hybridize in two natural hybrid zones show hybrid male sterility in laboratorial crosses. Using mitochondrial data, we infer that such populations have diverged some 100,000 years ago, surviving multiple glacial periods in isolated Pleistocenic refugia. Nuclear data shows that secondary contact has led to extensive introgression throughout the species range, including between populations showing hybrid male sterility. We find repeatable patterns of genomic differentiation across the two hybrid zones, yet such patterns are consistent with shared genomic constraints across taxa rather than their role in reproductive isolation. Together, our results suggest that Haldane’s rule can evolve relatively quickly within species, particularly when associated to strong demographic changes. At such early stages of species formation, hybrid male sterility still permits extensive gene flow, allowing future studies to identify genomic regions associated with reproductive barriers.

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Genetics of reproductive isolation in the Drosophila simulans clade: DNA marker-assisted mapping and characterization of a hybrid-male sterility gene, Odysseus (Ods).

Genetics ◽

10.1093/genetics/134.1.261 ◽

1993 ◽

Vol 134 (1) ◽

pp. 261-275 ◽

Cited By ~ 1

Author(s):

D E Perez ◽

C I Wu ◽

N A Johnson ◽

M L Wu

Keyword(s):

Male Sterility ◽

Major Gene ◽

Drosophila Simulans ◽

Recombination Analysis ◽

Hybrid Male ◽

Hybrid Male Sterility ◽

Complete Penetrance ◽

Drosophila Mauritiana ◽

Male Sterility Gene

Abstract In this study, we address the question of whether there exist major genes that cause complete male sterility in the interspecific hybrids of Drosophila and, if they do, how these genes may be characterized at the molecular level. Our approach is to introgress small segments of the X chromosome from Drosophila mauritiana (or Drosophila sechellia) into Drosophila simulans by repeated backcrosses for more than 20 generations. The introgressions are monitored by both visible mutations and a series of DNA markers. We compare the extent of introgressions that cause male sterility with those that do not. If a major sterility factor exists, there should be a sharp boundary between these two classes of introgressions and their breakpoints should demarcate such a gene. Furthermore, if male sterility is the only major fitness effect associated with the introgression, recombination analysis should yield a pattern predicted by the classical three-point cross. Both the genetic and molecular analyses suggest the presence of a major sterility factor from D. mauritiana, which we named Odysseus (Ods), in the cytological interval of 16D. We thus formalize three criteria for inferring the existence of a major gene within an introgression: (1) complete penetrance of sterility, (2) complementarity in recombination analysis, and (3) physical demarcation. Introgressions of Ods from D. sechellia do not cause sterility. Twenty-two introgressions in our collection have breakpoints in this interval of about 500 kb, making it possible to delineate Ods more precisely for molecular identification. The recombination analysis also reveals the complexity of the introgressed segments--even relatively short ones may contain a second male sterility factor and partial viability genes and may also interfere with crossovers. The spermatogenic defects associated with Ods and/or a second factor were characterized by phase-contrast microscopy.

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Hidden Effects of X Chromosome Introgressions on Spermatogenesis in Drosophila simulans × D. mauritiana Hybrids Unveiled by Interactions Among Minor Genetic Factors

Genetics ◽

10.1093/genetics/150.2.745 ◽

1998 ◽

Vol 150 (2) ◽

pp. 745-754 ◽

Cited By ~ 3

Author(s):

Xulio R Maside ◽

José P Barral ◽

Horacio F Naveira

Keyword(s):

Male Sterility ◽

X Chromosome ◽

Seminal Vesicles ◽

Genetic Dissection ◽

Research Strategies ◽

Hybrid Male ◽

Hybrid Male Sterility ◽

Epistatic Interactions ◽

Drosophila Mauritiana ◽

Chromosome Segments

Abstract One of the most frequent outcomes of interspecific hybridizations in Drosophila is hybrid male sterility. Genetic dissection of this reproductive barrier has revealed that the number of responsible factors is very high and that these factors are frequently engaged in complex epistatic interactions. Traditionally, research strategies have been based on contrasting introgressions of chromosome segments that produce male sterility with those that allow fertility. Few studies have investigated the phenotypes associated with the boundary between fertility and sterility. In this study, we cointrogressed three different X chromosome segments from Drosophila mauritiana into D. simulans. Hybrid males with these three segments are usually fertile, by conventional fertility assays. However, their spermatogenesis shows a significant slowdown, most manifest at lower temperatures. Each of the three introgressed segments retards the arrival of sperm to the seminal vesicles. Other small disturbances in spermatogenesis are evident, which altogether lead to an overall reduction in the amount of motile sperm in their seminal vesicles. These results suggest that a delay in the timing of spermatogenesis, which might be brought about by the cumulative action of many different factors of minor segment, may be the primary cause of hybrid male sterility.

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Hybrid Sterility, Genetic Conflict and Complex Speciation: Lessons From the Drosophila simulans Clade Species

Frontiers in Genetics ◽

10.3389/fgene.2021.669045 ◽

2021 ◽

Vol 12 ◽

Author(s):

Daven C. Presgraves ◽

Colin D. Meiklejohn

Keyword(s):

Gene Flow ◽

Male Sterility ◽

Hybrid Sterility ◽

Model Organism ◽

Drosophila Simulans ◽

Special Role ◽

Hybrid Male ◽

Hybrid Male Sterility ◽

Genetic Conflict ◽

Modern Evolutionary Synthesis

The three fruitfly species of the Drosophila simulans clade— D. simulans, D. mauritiana, and D. sechellia— have served as important models in speciation genetics for over 40 years. These species are reproductively isolated by geography, ecology, sexual signals, postmating-prezygotic interactions, and postzygotic genetic incompatibilities. All pairwise crosses between these species conform to Haldane’s rule, producing fertile F1 hybrid females and sterile F1 hybrid males. The close phylogenetic proximity of the D. simulans clade species to the model organism, D. melanogaster, has empowered genetic analyses of their species differences, including reproductive incompatibilities. But perhaps no phenotype has been subject to more continuous and intensive genetic scrutiny than hybrid male sterility. Here we review the history, progress, and current state of our understanding of hybrid male sterility among the D. simulans clade species. Our aim is to integrate the available information from experimental and population genetics analyses bearing on the causes and consequences of hybrid male sterility. We highlight numerous conclusions that have emerged as well as issues that remain unresolved. We focus on the special role of sex chromosomes, the fine-scale genetic architecture of hybrid male sterility, and the history of gene flow between species. The biggest surprises to emerge from this work are that (i) genetic conflicts may be an important general force in the evolution of hybrid incompatibility, (ii) hybrid male sterility is polygenic with contributions of complex epistasis, and (iii) speciation, even among these geographically allopatric taxa, has involved the interplay of gene flow, negative selection, and positive selection. These three conclusions are marked departures from the classical views of speciation that emerged from the modern evolutionary synthesis.

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The genetic basis of hybrid male sterility in sympatric Primulina species

BMC Evolutionary Biology ◽

10.1186/s12862-020-01617-4 ◽

2020 ◽

Vol 20 (1) ◽

Author(s):

Chen Feng ◽

Huiqin Yi ◽

Lihua Yang ◽

Ming Kang

Keyword(s):

Male Sterility ◽

Genetic Basis ◽

Hybrid Male ◽

Hybrid Male Sterility

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Interspecific Y chromosome variation is sufficient to rescue hybrid male sterility and is influenced by the grandparental origin of the chromosomes

Heredity ◽

10.1038/hdy.2016.11 ◽

2016 ◽

Vol 116 (6) ◽

pp. 516-522 ◽

Cited By ~ 7

Author(s):

L O Araripe ◽

Y Tao ◽

B Lemos

Keyword(s):

Male Sterility ◽

Y Chromosome ◽

Chromosome Variation ◽

Hybrid Male ◽

Hybrid Male Sterility

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The Contribution of the Y Chromosome to Hybrid Male Sterility in House Mice

Genetics ◽

10.1534/genetics.112.141804 ◽

2012 ◽

Vol 191 (4) ◽

pp. 1271-1281 ◽

Cited By ~ 17

Author(s):

Polly Campbell ◽

Jeffrey M. Good ◽

Matthew D. Dean ◽

Priscilla K. Tucker ◽

Michael W. Nachman

Keyword(s):

Male Sterility ◽

Y Chromosome ◽

House Mice ◽

Hybrid Male ◽

Hybrid Male Sterility

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Genetic basis to hybrid inviability is more complex than hybrid male sterility in Caenorhabditis nematodes

Heredity ◽

10.1038/s41437-018-0069-y ◽

2018 ◽

Vol 121 (2) ◽

pp. 169-182 ◽

Cited By ~ 6

Author(s):

Joanna D. Bundus ◽

Donglin Wang ◽

Asher D. Cutter

Keyword(s):

Male Sterility ◽

Genetic Basis ◽

Hybrid Male ◽

Hybrid Male Sterility ◽

Hybrid Inviability

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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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