scholarly journals Gene flow mediates the role of sex chromosome meiotic drive during complex speciation

2015 ◽  
Author(s):  
Colin D. Meiklejohn ◽  
Emily L. Landeen ◽  
Kathleen E. Gordon ◽  
Thomas Rzatkiewicz ◽  
Sarah B. Kingan ◽  
...  
Keyword(s):  
Gene Flow ◽  
Sex Chromosomes ◽  
Population Genomics ◽  
Sex Chromosome ◽  
Hybrid Sterility ◽  
Meiotic Drive ◽  
Hybrid Male ◽  
Selfish Genetic Elements ◽  
Cryptic Sex

ABSTRACTDuring speciation, sex chromosomes often accumulate interspecific genetic incompatibilities faster than the rest of the genome. The drive theory posits that sex chromosomes are susceptible to recurrent bouts of meiotic drive and suppression, causing the evolutionary build-up of divergent cryptic sex-linked drive systems and, incidentally, genetic incompatibilities. To assess the role of drive during speciation, we combine high-resolution genetic mapping of X-linked hybrid male sterility with population genomics analyses of divergence and recent gene flow between the fruitfly species, Drosophila mauritiana and D. simulans. Our findings reveal a high density of genetic incompatibilities and a corresponding dearth of gene flow on the X chromosome. Surprisingly, we find that, rather than contributing to interspecific divergence, a known drive element has recently migrated between species, caused a strong reduction in local divergence, and undermined the evolution of hybrid sterility. Gene flow can therefore mediate the effects of selfish genetic elements during speciation.

scholarly journals Gene flow mediates the role of sex chromosome meiotic drive during complex speciation

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Colin D Meiklejohn ◽  
Emily L Landeen ◽  
Kathleen E Gordon ◽  
Thomas Rzatkiewicz ◽  
Sarah B Kingan ◽  
...  
Keyword(s):  
Gene Flow ◽  
Sex Chromosomes ◽  
Population Genomics ◽  
Sex Chromosome ◽  
Hybrid Sterility ◽  
Sequence Divergence ◽  
Meiotic Drive ◽  
Hybrid Male ◽  
Local Sequence

During speciation, sex chromosomes often accumulate interspecific genetic incompatibilities faster than the rest of the genome. The drive theory posits that sex chromosomes are susceptible to recurrent bouts of meiotic drive and suppression, causing the evolutionary build-up of divergent cryptic sex-linked drive systems and, incidentally, genetic incompatibilities. To assess the role of drive during speciation, we combine high-resolution genetic mapping of X-linked hybrid male sterility with population genomics analyses of divergence and recent gene flow between the fruitfly species, Drosophila mauritiana and D. simulans. Our findings reveal a high density of genetic incompatibilities and a corresponding dearth of gene flow on the X chromosome. Surprisingly, we find that a known drive element recently migrated between species and, rather than contributing to interspecific divergence, caused a strong reduction in local sequence divergence, undermining the evolution of hybrid sterility. Gene flow can therefore mediate the effects of selfish genetic elements during speciation.

scholarly journals The role of meiotic drive in hybrid male sterility

2010 ◽  
Vol 365 (1544) ◽  
pp. 1265-1272 ◽  
Author(s):  
Shannon R. McDermott ◽  
Mohamed A. F. Noor
Keyword(s):  
Male Sterility ◽  
Hybrid Sterility ◽  
Meiotic Drive ◽  
Mechanistic Explanation ◽  
Hybrid Progeny ◽  
Hybrid Male ◽  
Hybrid Male Sterility ◽  
Species Formation ◽  
Allelic Segregation

Meiotic drive causes the distortion of allelic segregation away from Mendelian expected ratios, often also reducing fecundity and favouring the evolution of drive suppressors. If different species evolve distinct drive-suppressor systems, then hybrid progeny may be sterile as a result of negative interactions of these systems' components. Although the hypothesis that meiotic drive may contribute to hybrid sterility, and thus species formation, fell out of favour early in the 1990s, recent results showing an association between drive and sterility have resurrected this previously controversial idea. Here, we review the different forms of meiotic drive and their possible roles in speciation. We discuss the recent empirical evidence for a link between drive and hybrid male sterility, also suggesting a possible mechanistic explanation for this link in the context of chromatin remodelling. Finally, we revisit the population genetics of drive that allow it to contribute to speciation.

scholarly journals Author response: Gene flow mediates the role of sex chromosome meiotic drive during complex speciation

2018 ◽  
Author(s):  
Colin D Meiklejohn ◽  
Emily L Landeen ◽  
Kathleen E Gordon ◽  
Thomas Rzatkiewicz ◽  
Sarah B Kingan ◽  
...  
Keyword(s):  
Gene Flow ◽  
Sex Chromosome ◽  
Meiotic Drive ◽  
Author Response ◽  
Response Gene

scholarly journals Recurrent gene amplification on Drosophila Y chromosomes suggests cryptic sex chromosome drive is common on young sex chromosomes

2018 ◽  
Author(s):  
Chris Ellison ◽  
Doris Bachtrog
Keyword(s):  
Sex Chromosomes ◽  
Gene Pair ◽  
Sex Chromosome ◽  
Hybrid Sterility ◽  
Gene Families ◽  
Autosomal Gene ◽  
Evolutionary Patterns ◽  
Genetic Conflict ◽  
Chromosome Transmission ◽  
Cryptic Sex

Theory predicts that selfish genetic elements that increase their transmission are prone to originate on sex chromosomes but create strong selective pressure to evolve suppressors due to reduced fertility and distorted population sex ratios. Here we show that recurrent genetic conflict over sex chromosome transmission appears to be an important evolutionary force that has shaped gene content evolution of sex chromosomes in Drosophila. We demonstrate that convergent acquisition and amplification of spermatid expressed gene families are common on Drosophila sex chromosomes, and especially on recently formed ones, and harbor characteristics typical of meiotic drivers. We carefully characterize one putative novel cryptic sex chromosome distortion system that arose independently several times in members of the Drosophila obscura group. Co-amplification of the S-Lap1/GAPsec gene pair on both the X and the Y chromosome occurred independently several times in members of the D. obscura group, where this normally autosomal gene pair is sex-linked due to a sex chromosome - autosome fusion. Investigation of gene expression and short RNA profiles at the S-Lap1/GAPsec system suggest that meiotic drive and suppression likely involves RNAi mechanisms. Our finding suggests that recurrent conflict over sex chromosome transmission has shaped widespread genomic and evolutionary patterns, including the epigenetic regulation of sex chromosomes, the distribution of sex-biased genes, and the evolution of hybrid sterility.

Male Sterility and Meiotic Drive Associated With Sex Chromosome Rearrangements in Drosophila: Role of X-Y Pairing

Genetics ◽  
1998 ◽  
Vol 149 (1) ◽  
pp. 143-155 ◽  
Author(s):  
Bruce D McKee ◽  
Kathy Wilhelm ◽  
Cynthia Merrill ◽  
Xiao-jia Ren
Keyword(s):  
Male Sterility ◽  
Sex Chromosome ◽  
Meiotic Drive ◽  
Repeated Sequence ◽  
Meiotic Pairing ◽  
Intergenic Spacers ◽  
Male Specific ◽  
The Relationship ◽  
Novel Model

Abstract In Drosophila melanogaster, deletions of the pericentromeric X heterochromatin cause X-Y nondisjunction, reduced male fertility and distorted sperm recovery ratios (meiotic drive) in combination with a normal Y chromosome and interact with Y-autosome translocations (T(Y;A)) to cause complete male sterility. The pericentromeric heterochromatin has been shown to contain the male-specific X-Y meiotic pairing sites, which consist mostly of a 240-bp repeated sequence in the intergenic spacers (IGS) of the rDNA repeats. The experiments in this paper address the relationship between X-Y pairing failure and the meiotic drive and sterility effects of Xh deletions. X-linked insertions either of complete rDNA repeats or of rDNA fragments that contain the IGS were found to suppress X-Y nondisjunction and meiotic drive in Xh−/Y males, and to restore fertility to Xh−/T(Y;A) males for eight of nine tested Y-autosome translocations. rDNA fragments devoid of IGS repeats proved incapable of suppressing either meiotic drive or chromosomal sterility. These results indicate that the various spermatogenic disruptions associated with X heterochromatic deletions are all consequences of X-Y pairing failure. We interpret these findings in terms of a novel model in which misalignment of chromosomes triggers a checkpoint that acts by disabling the spermatids that derive from affected spermatocytes.

Introgression between non-sister species of honeyeaters (Aves: Meliphagidae) several million years after speciation

2019 ◽  
Vol 128 (3) ◽  
pp. 583-591
Author(s):  
Leo Joseph ◽  
Alex Drew ◽  
Ian J Mason ◽  
Jeffrey L Peters
Keyword(s):  
Gene Flow ◽  
Reproductive Isolation ◽  
Sex Chromosomes ◽  
Common Ancestor ◽  
Sister Species ◽  
Species Boundaries ◽  
North Eastern ◽  
The City

Abstract We reassessed whether two parapatric non-sister Australian honeyeater species (Aves: Meliphagidae), varied and mangrove honeyeaters (Gavicalis versicolor and G. fasciogularis, respectively), that diverged from a common ancestor c. 2.5 Mya intergrade in the Townsville area of north-eastern Queensland. Consistent with a previous specimen-based study, by using genomics methods we show one-way gene flow for autosomal but not Z-linked markers from varied into mangrove honeyeaters. Introgression barely extends south of the area of parapatry in and around the city of Townsville. While demonstrating the long-term porosity of species boundaries over several million years, our data also suggest a clear role of sex chromosomes in maintaining reproductive isolation.

scholarly journals Red queen's race: rapid evolutionary dynamics of an expanding family of meiotic drive factors and their hpRNA suppressors

2021 ◽  
Author(s):  
Jeffrey Vedanayagam ◽  
Ching-Jung Lin ◽  
Eric C. Lai
Keyword(s):  
Evolutionary Dynamics ◽  
Sex Chromosome ◽  
De Novo ◽  
Independent Set ◽  
Meiotic Drive ◽  
Sperm Chromatin ◽  
Arms Races ◽  
X Chromosomes ◽  
Selfish Genetic Elements ◽  
Satellite Repeats

Meiotic drivers are a class of selfish genetic elements that are widespread across eukaryotes. Their activities are often detrimental to organismal fitness and thus trigger drive suppression to ensure fair segregation during meiosis. Accordingly, their existence is frequently hidden in genomes, and their molecular functions are little known. Here, we trace evolutionary steps that generated the Dox meiotic drive system in Drosophila simulans (Dsim), which distorts male:female balance (sex-ratio) by depleting male progeny. We show that Dox emerged via stepwise mobilization and acquisition of portions of multiple D. melanogaster genes, including the sperm chromatin packaging gene protamine. Moreover, we reveal novel Dox homologs in Dsim and massive, recent, amplification of Dox superfamily genes specifically on X chromosomes of its closest sister species D. mauritiana (Dmau) and D. sechellia (Dsech). The emergence of Dox superfamily genes is tightly associated with 1.688 family satellite repeats that flank de novo genomic copies. In concert, we find coordinated emergence and diversification of autosomal hairpin RNA/siRNAs loci that target subsets of Dox superfamily genes across simulans clade species. Finally, an independent set of protamine amplifications the Y chromosome of D. melanogaster indicates that protamine genes are frequent and recurrent players in sex chromosome dynamics. Overall, we reveal fierce genetic arms races between meiotic drive factors and siRNA suppressors associated with recent speciation.

scholarly journals Sex chromosome evolution: historical insights and future perspectives

2017 ◽  
Vol 284 (1854) ◽  
pp. 20162806 ◽  
Author(s):  
Jessica K. Abbott ◽  
Anna K. Nordén ◽  
Bengt Hansson
Keyword(s):  
Sex Determination ◽  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Empirical Studies ◽  
Analytical Models ◽  
Specific Gene ◽  
Sex Chromosome Evolution ◽  
Current Thinking

Many separate-sexed organisms have sex chromosomes controlling sex determination. Sex chromosomes often have reduced recombination, specialized (frequently sex-specific) gene content, dosage compensation and heteromorphic size. Research on sex determination and sex chromosome evolution has increased over the past decade and is today a very active field. However, some areas within the field have not received as much attention as others. We therefore believe that a historic overview of key findings and empirical discoveries will put current thinking into context and help us better understand where to go next. Here, we present a timeline of important conceptual and analytical models, as well as empirical studies that have advanced the field and changed our understanding of the evolution of sex chromosomes. Finally, we highlight gaps in our knowledge so far and propose some specific areas within the field that we recommend a greater focus on in the future, including the role of ecology in sex chromosome evolution and new multilocus models of sex chromosome divergence.

scholarly journals Sex chromosome evolution among amniotes: is the origin of sex chromosomes non-random?

2021 ◽  
Vol 376 (1833) ◽  
pp. 20200108 ◽  
Author(s):  
Lukáš Kratochvíl ◽  
Tony Gamble ◽  
Michail Rovatsos
Keyword(s):  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Current Knowledge ◽  
Current Data ◽  
Divergent Evolution ◽  
Random Pattern ◽  
Sex Chromosome Evolution ◽  
Great Opportunity

Sex chromosomes are a great example of a convergent evolution at the genomic level, having evolved dozens of times just within amniotes. An intriguing question is whether this repeated evolution was random, or whether some ancestral syntenic blocks have significantly higher chance to be co-opted for the role of sex chromosomes owing to their gene content related to gonad development. Here, we summarize current knowledge on the evolutionary history of sex determination and sex chromosomes in amniotes and evaluate the hypothesis of non-random emergence of sex chromosomes. The current data on the origin of sex chromosomes in amniotes suggest that their evolution is indeed non-random. However, this non-random pattern is not very strong, and many syntenic blocks representing putatively independently evolved sex chromosomes are unique. Still, repeatedly co-opted chromosomes are an excellent model system, as independent co-option of the same genomic region for the role of sex chromosome offers a great opportunity for testing evolutionary scenarios on the sex chromosome evolution under the explicit control for the genomic background and gene identity. Future studies should use these systems more to explore the convergent/divergent evolution of sex chromosomes. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)’.

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