Sex chromosome inversions enforce reproductive isolation across an avian hybrid zone

2018 ◽  
Vol 28 (6) ◽  
pp. 1246-1262 ◽  
Author(s):  
Daniel M. Hooper ◽  
Simon C. Griffith ◽  
Trevor D. Price
Keyword(s):  
Reproductive Isolation ◽  
Hybrid Zone ◽  
Sex Chromosome ◽  
Chromosome Inversions

scholarly journals X-Linked Signature of Reproductive Isolation in Humans is Mirrored in a Howler Monkey Hybrid Zone

2020 ◽  
Vol 111 (5) ◽  
pp. 419-428 ◽  
Author(s):  
Marcella D Baiz ◽  
Priscilla K Tucker ◽  
Jacob L Mueller ◽  
Liliana Cortés-Ortiz
Keyword(s):  
Reproductive Isolation ◽  
X Chromosome ◽  
Hybrid Zone ◽  
Sex Chromosome ◽  
Genomic Sequence ◽  
Alouatta Palliata ◽  
Model Systems ◽  
Howler Monkey ◽  
Autosomal Snps ◽  
Outlier Region

Abstract Reproductive isolation is a fundamental step in speciation. While sex chromosomes have been linked to reproductive isolation in many model systems, including hominids, genetic studies of the contribution of sex chromosome loci to speciation for natural populations are relatively sparse. Natural hybrid zones can help identify genomic regions contributing to reproductive isolation, like hybrid incompatibility loci, since these regions exhibit reduced introgression between parental species. Here, we use a primate hybrid zone (Alouatta palliata × Alouatta pigra) to test for reduced introgression of X-linked SNPs compared to autosomal SNPs. To identify X-linked sequence in A. palliata, we used a sex-biased mapping approach with whole-genome re-sequencing data. We then used genomic cline analysis with reduced-representation sequence data for parental A. palliata and A. pigra individuals and hybrids (n = 88) to identify regions with non-neutral introgression. We identified ~26 Mb of non-repetitive, putatively X-linked genomic sequence in A. palliata, most of which mapped collinearly to the marmoset and human X chromosomes. We found that X-linked SNPs had reduced introgression and an excess of ancestry from A. palliata as compared to autosomal SNPs. One outlier region with reduced introgression overlaps a previously described “desert” of archaic hominin ancestry on the human X chromosome. These results are consistent with a large role for the X chromosome in speciation across animal taxa and further, suggest shared features in the genomic basis of the evolution of reproductive isolation in primates.

scholarly journals Network Analysis of Linkage Disequilibrium Reveals Genome Architecture in Chum Salmon

2020 ◽  
Vol 10 (5) ◽  
pp. 1553-1561 ◽  
Author(s):  
Garrett McKinney ◽  
Megan V. McPhee ◽  
Carita Pascal ◽  
James E. Seeb ◽  
Lisa W. Seeb
Keyword(s):  
Population Structure ◽  
Linkage Disequilibrium ◽  
Network Analysis ◽  
Chum Salmon ◽  
Sex Chromosome ◽  
Natural Populations ◽  
Population Substructure ◽  
Chromosome Inversion ◽  
Genomic Features ◽  
Chromosome Inversions

Many studies exclude loci that exhibit linkage disequilibrium (LD); however, high LD can signal reduced recombination around genomic features such as chromosome inversions or sex-determining regions. Chromosome inversions and sex-determining regions are often involved in adaptation, allowing for the inheritance of co-adapted gene complexes and for the resolution of sexually antagonistic selection through sex-specific partitioning of genetic variants. Genomic features such as these can escape detection when loci with LD are removed; in addition, failing to account for these features can introduce bias to analyses. We examined patterns of LD using network analysis to identify an overlapping chromosome inversion and sex-determining region in chum salmon. The signal of the inversion was strong enough to show up as false population substructure when the entire dataset was analyzed, while the effect of the sex-determining region on population structure was only obvious after restricting analysis to the sex chromosome. Understanding the extent and geographic distribution of inversions is now a critically important part of genetic analyses of natural populations. Our results highlight the importance of analyzing and understanding patterns of LD in genomic dataset and the perils of excluding or ignoring loci exhibiting LD. Blindly excluding loci in LD would have prevented detection of the sex-determining region and chromosome inversion while failing to understand the genomic features leading to high-LD could have resulted in false interpretations of population structure.

scholarly journals Ancestral and neo-sex chromosomes contribute to population divergence in a dioecious plant

2019 ◽  
Author(s):  
Felix E.G. Beaudry ◽  
Spencer C.H. Barrett ◽  
Stephen I. Wright
Keyword(s):  
Gene Flow ◽  
Reproductive Isolation ◽  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Demographic History ◽  
Population Divergence ◽  
Effective Population ◽  
Dioecious Plant ◽  
Fusion Event ◽  
Contemporary Gene Flow

ABSTRACTEmpirical evidence from several animal groups suggests that sex chromosomes may disproportionately contribute to reproductive isolation. This occurs particularly when sex chromosomes are associated with turnover of sex determination systems resulting from structural rearrangements to the sex chromosomes. We investigated these predictions in the dioecious plant Rumex hastatulus, which is comprised of populations of two sex chromosome cytotypes. Using population genomic analyses, we investigated the demographic history of R. hastatulus and explored the contributions of ancestral and neo-sex chromosomes to population genetic divergence. Our study revealed that the cytotypes represented genetically divergent populations with evidence for historical but not contemporary gene flow between them. In agreement with classical predictions, we found that the ancestral X chromosome was disproportionately divergent compared with the rest of the genome. Excess differentiation was also observed on the Y chromosome, even when using measures of differentiation that control for differences in effective population size. Our estimates of the timing of the origin of the neo-sex chromosomes in R. hastatulus are coincident with cessation of gene flow, suggesting that the chromosomal fusion event that gave rise to the origin of the XYY cytotype may have also been a key driver of reproductive isolation.

scholarly journals Population genomic evidence of selection on structural variants in a natural hybrid zone

2022 ◽  
Author(s):  
Linyi Zhang ◽  
Samridhi Chaturvedi ◽  
Chris Nice ◽  
Lauren Lucas ◽  
Zachariah Gompert
Keyword(s):  
Reproductive Isolation ◽  
Hybrid Zone ◽  
Structural Variants ◽  
Hybrid Fitness ◽  
Genome Wide ◽  
Oxford Nanopore ◽  
Jackson Hole ◽  
Long Read ◽  
Genomic Regions

Structural variants (SVs) can promote speciation by directly causing reproductive isolation or by suppressing recombination across large genomic regions. Whereas examples of each mechanism have been documented, systematic tests of the role of SVs in speciation are lacking. Here, we take advantage of long-read (Oxford nanopore) whole-genome sequencing and a hybrid zone between two Lycaeides butterfly taxa (L. melissa and Jackson Hole Lycaeides) to comprehensively evaluate genome-wide patterns of introgression for SVs and relate these patterns to hypotheses about speciation. We found >100,000 SVs segregating within or between the two hybridizing species. SVs and SNPs exhibited similar levels of genetic differentiation between species, with the exception of inversions, which were more differentiated. We detected credible variation in patterns of introgression among SV loci in the hybrid zone, with 562 of 1419 ancestry-informative SVs exhibiting genomic clines that deviating from null expectations based on genome-average ancestry. Overall, hybrids exhibited a directional shift towards Jackson Hole Lycaeides ancestry at SV loci, consistent with the hypothesis that these loci experienced more selection on average then SNP loci. Surprisingly, we found that deletions, rather than inversions, showed the highest skew towards excess introgression from Jackson Hole Lycaeides. Excess Jackson Hole Lycaeides ancestry in hybrids was also especially pronounced for Z-linked SVs and inversions containing many genes. In conclusion, our results show that SVs are ubiquitous and suggest that SVs in general, but especially deletions, might contribute disproportionately to hybrid fitness and thus (partial) reproductive isolation.

scholarly journals Sex chromosomes in meiotic, hemiclonal, clonal and polyploid hybrid vertebrates: along the ‘extended speciation continuum'

2021 ◽  
Vol 376 (1833) ◽  
pp. 20200103 ◽  
Author(s):  
Matthias Stöck ◽  
Dmitrij Dedukh ◽  
Radka Reifová ◽  
Dunja K. Lamatsch ◽  
Zuzana Starostová ◽  
...  
Keyword(s):  
Reproductive Isolation ◽  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Dominance Hierarchies ◽  
Speciation Continuum ◽  
Well Differentiated ◽  
Evolution Understanding ◽  
Meiotic Aberrations ◽  
Male Heterogamety

We review knowledge about the roles of sex chromosomes in vertebrate hybridization and speciation, exploring a gradient of divergences with increasing reproductive isolation (speciation continuum). Under early divergence, well-differentiated sex chromosomes in meiotic hybrids may cause Haldane-effects and introgress less easily than autosomes. Undifferentiated sex chromosomes are more susceptible to introgression and form multiple (or new) sex chromosome systems with hardly predictable dominance hierarchies. Under increased divergence, most vertebrates reach complete intrinsic reproductive isolation. Slightly earlier, some hybrids (linked in ‘the extended speciation continuum') exhibit aberrant gametogenesis, leading towards female clonality. This facilitates the evolution of various allodiploid and allopolyploid clonal (‘asexual’) hybrid vertebrates, where ‘asexuality' might be a form of intrinsic reproductive isolation. A comprehensive list of ‘asexual' hybrid vertebrates shows that they all evolved from parents with divergences that were greater than at the intraspecific level (K2P-distances of greater than 5–22% based on mtDNA). These ‘asexual' taxa inherited genetic sex determination by mostly undifferentiated sex chromosomes. Among the few known sex-determining systems in hybrid ‘asexuals', female heterogamety (ZW) occurred about twice as often as male heterogamety (XY). We hypothesize that pre-/meiotic aberrations in all-female ZW-hybrids present Haldane-effects promoting their evolution. Understanding the preconditions to produce various clonal or meiotic allopolyploids appears crucial for insights into the evolution of sex, ‘asexuality' and polyploidy. 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)’.

Sex-Chromosome Inversions in Chironomus

1957 ◽  
Vol 91 (856) ◽  
pp. 57-59 ◽  
Author(s):  
A. B. Acton
Keyword(s):  
Sex Chromosome ◽  
Chromosome Inversions

scholarly journals Extensive Recombination Suppression and Epistatic Selection Causes Chromosome-Wide Differentiation of a Selfish Sex Chromosome in Drosophila pseudoobscura

Genetics ◽  
2020 ◽  
Vol 216 (1) ◽  
pp. 205-226 ◽  
Author(s):  
Zachary L. Fuller ◽  
Spencer A. Koury ◽  
Christopher J. Leonard ◽  
Randee E. Young ◽  
Kobe Ikegami ◽  
...  
Keyword(s):  
Population Genetic ◽  
Sex Chromosome ◽  
Chromosomal Rearrangements ◽  
Comparative Genomic ◽  
Recombination Suppression ◽  
Mendelian Segregation ◽  
Multiple Alleles ◽  
Chromosome Inversions ◽  
Combined Action ◽  
The Right

Sex-Ratio (SR) chromosomes are selfish X-chromosomes that distort Mendelian segregation and are commonly associated with inversions. These chromosomal rearrangements suppress recombination with Standard (ST) X-chromosomes and are hypothesized to maintain multiple alleles important for distortion in a single large haplotype. Here, we conduct a multifaceted study of the multiply inverted Drosophila pseudoobscura SR chromosome to understand the evolutionary history, genetic architecture, and present-day dynamics that shape this enigmatic selfish chromosome. The D. pseudoobscura SR chromosome has three nonoverlapping inversions of the right arm of the metacentric X-chromosome: basal, medial, and terminal. We find that 23 of 29 Mb of the D. pseudoobscuraX-chromosome right arm is highly differentiated between the Standard and SR arrangements, including a 6.6 Mb collinear region between the medial and terminal inversions. Although crossing-over is heavily suppressed on this chromosome arm, we discover it is not completely eliminated, with measured rates indicating recombination suppression alone cannot explain patterns of differentiation or the near-perfect association of the three SR chromosome inversions in nature. We then demonstrate the ancient basal and medial inversions of the SR chromosome contain genes sufficient to cause weak distortion. In contrast, the younger terminal inversion cannot distort by itself, but contains at least one modifier gene necessary for full manifestation of strong sex chromosome distortion. By parameterizing population genetic models for chromosome-wide linkage disequilibrium with our experimental results, we infer that strong selection acts to maintain the near-perfect association of SR chromosome inversions in present-day populations. Based on comparative genomic analyses, direct recombination experiments, segregation distortion assays, and population genetic modeling, we conclude the combined action of suppressed recombination and strong, ongoing, epistatic selection shape the D. pseudoobscura SR arrangement into a highly differentiated chromosome.

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