Evolution of Postmating Reproductive Isolation: Measuring the Fitness Effects of Chromosomal Regions Containing Hybrid Male Sterility Factors

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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Age and genetic background determine hybrid male sterility in house mice

10.1101/382382 ◽

2018 ◽

Author(s):

Samuel J. Widmayer ◽

David L. Aylor

Keyword(s):

Reproductive Isolation ◽

Male Sterility ◽

Genetic Factors ◽

Inbred Strains ◽

House Mice ◽

Reproductive Barriers ◽

Hybrid Male ◽

Hybrid Male Sterility ◽

Unique Type ◽

Age Dependent

AbstractHybrid male sterility (HMS) is a unique type of reproductive isolation commonly observed between house mouse (Mus musculus) subspecies in the wild and in laboratory crosses. We identified hybrids that display three distinct trajectories of fertility despite having identical genotypes at the major HMS gene Prdm9 and the X Chromosome. In each case, we crossed female PWK/PhJ mice representative of the M.m.musculus subspecies to males from classical inbred strains representative of M.m.domesticus: 129S1/SvImJ, A/J, C57BL/6J, and DBA/2J. PWK129S1 males are always sterile, while PWKDBA2 males escape HMS. In addition, we observe age-dependent sterility in PWKB6 and PWKAJ males. These males are fertile between 15 and 35 weeks with moderate penetrance. These results point to multiple segregating HMS modifier alleles, some of which have an age-dependent mode of action. Age-dependent mechanisms could have broad implications for the maintenance of reproductive barriers in nature.Author SummaryTwo subspecies of house mice show partial reproductive barriers in nature, and may be in the process of speciation. We used mice derived from each subspecies to replicate hybrid male sterility (HMS) in laboratory mice. Two major genetic factors are well established as playing a role in mouse HMS, but the number of additional factors and their mechanisms are unknown. We characterized reproductive trait variation in a set of hybrid male mice that were specifically designed to eliminate the effects of known genetic factors. We discovered that age played an important role in fertility of some hybrids. These hybrid males showed a delayed onset of fertility, then became fertile for only a few weeks. Across all hybrids males in our study, we observed three distinct trajectories of fertility: complete fertility, complete sterility, and age-dependent fertility. These results point to two or more critical HMS variants with large enough effects to completely restore fertility. This study advances our understanding of the genetic architecture and biological mechanisms of reproductive isolation in mice.

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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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The Genetic Basis of Postzygotic Reproductive Isolation Between Drosophila santomea and D. yakuba Due to Hybrid Male Sterility

Genetics ◽

10.1534/genetics.105.052985 ◽

2006 ◽

Vol 173 (1) ◽

pp. 225-233 ◽

Cited By ~ 51

Author(s):

Amanda J. Moehring ◽

Ana Llopart ◽

Susannah Elwyn ◽

Jerry A. Coyne ◽

Trudy F. C. Mackay

Keyword(s):

Reproductive Isolation ◽

Male Sterility ◽

Genetic Basis ◽

Hybrid Male ◽

Hybrid Male Sterility ◽

Postzygotic Reproductive Isolation

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The Genetics of Reproductive Isolation in the Drosophila simulans Clade: X vs. Autosomal Effects and Male vs. Female Effects

Genetics ◽

10.1093/genetics/143.3.1243 ◽

1996 ◽

Vol 143 (3) ◽

pp. 1243-1255 ◽

Cited By ~ 1

Author(s):

Hope Hollocher ◽

Chug-I Wu

Keyword(s):

Reproductive Isolation ◽

Male Sterility ◽

X Chromosome ◽

Hybrid Sterility ◽

Drosophila Simulans ◽

Female Sterility ◽

Hybrid Male ◽

Hybrid Female ◽

Hybrid Male Sterility ◽

Hybrid Inviability

Abstract A strong effect of homozygous autosomal regions on reproductive isolation was found for crosses between the species in the Drosophila simulans clade. Second chromosome regions were introgressed from D. mauritiana and D. sechellia into D. simulans and tested for their homozygous effects on hybrid male and hybrid female sterility and inviability. Most introgressions are fertile as heterozygotes, yet produce sterile male offspring when made homozygous. The density of homozygous autosomal factors contributing to hybrid male sterility is comparable to the density of X chromosome factors for this level of resolution. Female sterility was also revealed, yet the disparity between male and female levels of sterility was great, with male sterility being up to 23 times greater than female sterility. Complete hybrid inviability was also associated with some regions of the second chromosome, yet there were no strong sex differences. In conclusion, we find no evidence to support a strong X chromosome bias in the evolution of hybrid sterility or inviability but do find a very strong sex bias in the evolution of hybrid sterility. In light of these findings, we reevaluate the current models proposed to explain the genetic pattern of reproductive isolation.

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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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