A common suite of cellular abnormalities and spermatogenetic errors in sterile hybrid males in
            Drosophila

When two species interbreed, the resulting hybrid offspring are often sterile, with the heterogametic (e.g. XY) hybrid usually being more severely affected. The prevailing theory for this pattern of sterility evokes divergent changes in separate lineages having maladaptive interactions when placed together in a hybrid individual, with recessive factors on the sex chromosome interacting with dominant factors on the autosomes. The effect of these interactions on gametogenesis should not be uniform across species pairs unless genetic divergence follows the same paths in different lineages or if a specific stage of gametogenesis is more susceptible to detrimental genetic interactions. Here, we perform a detailed cellular characterization of hybrid male sterility across three recently diverged species pairs of Drosophila . Across all three pairs, sterile hybrid sperm are alive but exhibit rapid nuclear de-condensation with age, with active, but non-differentiated, mitochondria. Surprisingly, all three sets of interspecies hybrids produce half of the number of sperm per round of spermatogenesis, with each sperm cell containing two tails. We identify non-disjunction failures during meiosis I as the likely cause. Thus, errors during meiosis I may be a general phenomenon underlying Drosophila male sterility, indicating either a heightened sensitivity of this spermatogenic stage to failure, or a basis to sterility other than the prevailing model.

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Cytological Characterization of Premeiotic Versus Postmeiotic Defects Producing Hybrid Male Sterility among Sibling Species of the Drosophila melanogaster Complex

Evolution ◽

10.2307/2411237 ◽

1998 ◽

Vol 52 (4) ◽

pp. 1067 ◽

Cited By ~ 12

Author(s):

Rob Kulathinal ◽

Rama S. Singh

Keyword(s):

Drosophila Melanogaster ◽

Male Sterility ◽

Sibling Species ◽

Hybrid Male ◽

Hybrid Male Sterility

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CYTOLOGICAL CHARACTERIZATION OF PREMEIOTIC VERSUS POSTMEIOTIC DEFECTS PRODUCING HYBRID MALE STERILITY AMONG SIBLING SPECIES OF THE DROSOPHILA MELANOGASTER COMPLEX

Evolution ◽

10.1111/j.1558-5646.1998.tb01834.x ◽

1998 ◽

Vol 52 (4) ◽

pp. 1067-1079 ◽

Cited By ~ 13

Author(s):

Rob Kulathinal ◽

Rama S. Singh

Keyword(s):

Drosophila Melanogaster ◽

Male Sterility ◽

Sibling Species ◽

Hybrid Male ◽

Hybrid Male Sterility

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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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Faculty Opinions recommendation of Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.717963248.793465268 ◽

2012 ◽

Author(s):

John Willis

Keyword(s):

Male Sterility ◽

Hybrid Male ◽

Hybrid Male Sterility

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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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Genetic Complexity Underlying Hybrid Male Sterility in Drosophila

Genetics ◽

10.1093/genetics/166.2.789 ◽

2004 ◽

Vol 166 (2) ◽

pp. 789-796 ◽

Cited By ~ 1

Author(s):

Kyoichi Sawamura ◽

John Roote ◽

Chung-I Wu ◽

Masa-Toshi Yamamoto

Keyword(s):

Male Sterility ◽

Related Species ◽

Synergistic Effects ◽

Female Sterility ◽

Hybrid Male ◽

Hybrid Female ◽

Hybrid Male Sterility ◽

Closely Related Species ◽

Genetic Complexity ◽

Recessive Genes

Abstract Recent genetic analyses of closely related species of Drosophila have indicated that hybrid male sterility is the consequence of highly complex synergistic effects among multiple genes, both conspecific and heterospecific. On the contrary, much evidence suggests the presence of major genes causing hybrid female sterility and inviability in the less-related species, D. melanogaster and D. simulans. Does this contrast reflect the genetic distance between species? Or, generally, is the genetic basis of hybrid male sterility more complex than that of hybrid female sterility and inviability? To clarify this point, the D. simulans introgression of the cytological region 34D-36A to the D. melanogaster genome, which causes recessive male sterility, was dissected by recombination, deficiency, and complementation mapping. The 450-kb region between two genes, Suppressor of Hairless and snail, exhibited a strong effect on the sterility. Males are (semi-)sterile if this region of the introgression is made homozygous or hemizygous. But no genes in the region singly cause the sterility; this region has at least two genes, which in combination result in male sterility. Further, the males are less fertile when heterozygous with a larger introgression, which suggests that dominant modifiers enhance the effects of recessive genes of male sterility. Such an epistatic view, even in the less-related species, suggests that the genetic complexity is special to hybrid male sterility.

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Age and genetic background modify hybrid male sterility in house mice

10.1101/2020.06.26.173047 ◽

2020 ◽

Author(s):

Samuel J. Widmayer ◽

Mary Ann Handel ◽

David L. Aylor

Keyword(s):

Male Sterility ◽

House Mouse ◽

Genetic Background ◽

Genetic Architecture ◽

Hybrid Male ◽

Hybrid Male Sterility ◽

X Chromosomes ◽

Age Related ◽

Age Dependent ◽

In The Wild

AbstractHybrid male sterility (HMS) contributes to reproductive isolation commonly observed among house mouse (Mus musculus) subspecies, both in the wild and in laboratory crosses. Incompatibilities involving specific Prdm9 alleles and certain Chromosome (Chr) X genotypes are known determinants of fertility and HMS, and previous work in the field has demonstrated that genetic background modifies these two major loci. We constructed hybrids that have identical genotypes at Prdm9 and identical X chromosomes, but differ widely across the rest of the genome. In each case, we crossed female PWK/PhJ mice representative of the M. m. musculus subspecies to males from a classical inbred strain representative of M. m. domesticus: 129S1/SvImJ, A/J, C57BL/6J, or DBA/2J. We detected three distinct trajectories of fertility among the hybrids using breeding experiments. The PWK129S1 males were always infertile. PWKDBA2 males were fertile, despite their genotypes at the major HMS loci. We also observed age-dependent changes in fertility parameters across multiple genetic backgrounds. The PWKB6 and PWKAJ males were always infertile before 15 weeks and after 35 weeks, yet some PWKB6 and PWKAJ males were fertile between fifteen and 35 weeks. This observation could resolve previous contradictory reports about the fertility of PWKB6. Taken together, these results point to multiple segregating HMS modifier alleles, some of which have age-related modes of action. The ultimate identification of these alleles and their age-related mechanisms will advance understanding both of the genetic architecture of HMS and of how reproductive barriers are maintained between house mouse subspecies.

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Specific Interactions Between Autosome and X Chromosomes Cause Hybrid Male Sterility in Caenorhabditis Species

Genetics ◽

10.1534/genetics.119.302202 ◽

2019 ◽

Vol 212 (3) ◽

pp. 801-813 ◽

Cited By ~ 4

Author(s):

Yu Bi ◽

Xiaoliang Ren ◽

Runsheng Li ◽

Qiutao Ding ◽

Dongying Xie ◽

...

Keyword(s):

Male Sterility ◽

Male Fertility ◽

Genetic Mechanism ◽

Hybrid Male ◽

Female Progeny ◽

Hybrid Male Sterility ◽

Male And Female ◽

F1 Progeny ◽

Asymmetric Hybrid ◽

Parent Of Origin

Hybrid male progeny from interspecies crosses are more prone to sterility or inviability than hybrid female progeny, and the male sterility and inviability often demonstrate parent-of-origin asymmetry. However, the underlying genetic mechanism of asymmetric sterility or inviability remains elusive. We previously established a genome-wide hybrid incompatibility (HI) landscape between Caenorhabditis briggsae and C. nigoni by phenotyping a large collection of C. nigoni strains each carrying a C. briggsae introgression. In this study, we systematically dissect the genetic mechanism of asymmetric sterility and inviability in both hybrid male and female progeny between the two species. Specifically, we performed reciprocal crosses between C. briggsae and different C. nigoni strains that each carry a GFP-labeled C. briggsae genomic fragment referred to as introgression, and scored the HI phenotypes in the F1 progeny. The aggregated introgressions cover 94.6% of the C. briggsae genome, including 100% of the X chromosome. Surprisingly, we observed that two C. briggsaeX fragments that produce C. nigoni male sterility as an introgression rescued hybrid F1 sterility in males fathered by C. briggsae. Subsequent backcrossing analyses indicated that a specific interaction between the X-linked interaction and one autosome introgression is required to rescue the hybrid male sterility. In addition, we identified another two C. briggsae genomic intervals on chromosomes II and IV that can rescue the inviability, but not the sterility, of hybrid F1 males fathered by C. nigoni, suggesting the involvement of differential epistatic interactions in the asymmetric hybrid male fertility and inviability. Importantly, backcrossing of the rescued sterile males with C. nigoni led to the isolation of a 1.1-Mb genomic interval that specifically interacts with an X-linked introgression, which is essential for hybrid male fertility. We further identified three C. briggsae genomic intervals on chromosome I, II, and III that produced inviability in all F1 progeny, dependent on or independent of the parent-of-origin. Taken together, we identified multiple independent interacting loci that are responsible for asymmetric hybrid male and female sterility, and inviability, which lays a foundation for their molecular characterization.

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