Premeiotic and meiotic failures lead to hybrid male sterility in the
            Anopheles gambiae
            complex

Hybrid male sterility (HMS) contributes to speciation by restricting gene flow between related taxa. Detailed cytological characterization of reproductive organs in hybrid males is important for identifying phenotypes that can help guide searches of speciation genes. To investigate possible cellular causes of HMS, we performed crosses between closely related species of the Anopheles gambiae complex: An. merus with An. gambiae or An. coluzzii . We demonstrate that HMS in African malaria mosquitoes involves two defects in the reciprocal crosses: a premeiotic arrest of germline stem cells in degenerate testes and a failure of the reductional meiotic division of primary spermatocytes in normal-like testes. The premeiotic arrest in degenerate testes of hybrids is accompanied by a strong suppression of meiotic and postmeiotic genes. Unlike pure species, sex chromosomes in normal-like testes of F1 hybrids are largely unpaired during meiotic prophase I and all chromosomes show various degrees of insufficient condensation. Instead of entering reductional division in meiosis I, primary spermatocytes prematurely undergo an equational mitotic division producing non-motile diploid sperm. Thus, our study identified cytogenetic errors in interspecies hybrids that arise during the early stages of postzygotic isolation.

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Premeiotic and meiotic failures lead to hybrid male sterility in the Anopheles gambiae complex

10.1101/507889 ◽

2018 ◽

Author(s):

Jiangtao Liang ◽

Igor V. Sharakhov

Keyword(s):

Anopheles Gambiae ◽

Male Sterility ◽

Reproductive Organs ◽

Mitotic Division ◽

F1 Hybrids ◽

Germline Stem Cells ◽

Hybrid Male ◽

Strong Suppression ◽

Hybrid Male Sterility ◽

Pure Species

AbstractHybrid male sterility contributes to speciation by restricting gene flow between related taxa. Detailed cytological characterizations of reproductive organs in hybrid males is important for identifying phenotypes that can help guide searches of speciation genes. To investigate possible cellular causes of hybrid male sterility, we performed crosses between closely related species of the Anopheles gambiae complex: An. merus with An. gambiae or An. coluzzii. We demonstrate that hybrid male sterility in African malaria mosquitoes involves two defects in the reciprocal crosses: a premeiotic arrest of germline stem cells in degenerate testes and a failure of the reductional meiotic division of primary spermatocytes in normal-like testes. The premeiotic arrest in degenerate testes of hybrids is accompanied by a strong suppression of meiotic and postmeiotic genes. Unlike pure species, sex chromosomes in normal-like testes of F1 hybrids are largely unpaired during meiotic prophase I and all chromosomes show various degrees of insufficient condensation. Instead of entering reductional division in meiosis I, primary spermatocytes prematurely undergo an equational mitotic division producing nonmotile diploid sperm. Thus, our study identified cytogenetic errors in interspecies hybrids that arise during the early stages of postzygotic isolation.

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Evaluation of the courtship and of the hybrid male sterility among Drosophila buzzatii cluster species (Diptera, Drosophilidae)

Brazilian Journal of Biology ◽

10.1590/s1519-69842002000400007 ◽

2002 ◽

Vol 62 (4a) ◽

pp. 601-608 ◽

Cited By ~ 1

Author(s):

L. P. de B. MACHADO ◽

J. P.de CASTRO ◽

L. MADI-RAVAZZI

Keyword(s):

Reproductive Isolation ◽

Male Sterility ◽

F1 Hybrids ◽

Interspecific Crosses ◽

Hybrid Male ◽

Hybrid Male Sterility ◽

Drosophila Buzzatii ◽

Repleta Group ◽

Reproductive Isolation Mechanisms ◽

Isolation Mechanisms

In the Drosophila repleta group the establishment of subgroups and complexes made on the basis of morphological and cytological evidences is supported by tests of reproductive isolation. Among species in the repleta group, the buzzatii cluster, due to its polymorphism and polytipism, is an excellent material for ecological and speciation studies. Some interspecific crosses involving Drosophila seriema, Drosophila sp. B, D. koepferae and D. buzzatii strains were completely sterile while others involving strains from these species produced F1 hybrids that did not yield F2. In the present work, data on courtship duration and copula occurrence obtained in the analysis of flies from parental sterile crosses and on spermatozoon mobility observed in F1 hybrids that did not yield F2 are presented. Copula did not occur during one hour of observation and the spermatozoon also did not show mobility at any of the analyzed stages (3, 7, 9 and 10 days old). There was a high variation in courtship average duration and in the percentage of males that courted the females. The reproductive isolation mechanisms indicated by these observations were pre and post-zygotic, as supported by the absence of copula and male sterility. Data obtained also showed the occurrence of different degrees of reproductive compatibility among the strains classified as the same species but from distinct geographic localities.

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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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