scholarly journals The avian W chromosome is a refugium for endogenous retroviruses with likely effects on female-biased mutational load and genetic incompatibilities

2021 ◽  
Vol 376 (1833) ◽  
pp. 20200186
Author(s):  
Valentina Peona ◽  
Octavio M. Palacios-Gimenez ◽  
Julie Blommaert ◽  
Jing Liu ◽  
Tri Haryoko ◽  
...  
Keyword(s):  
Sex Chromosome ◽  
Gene Dosage ◽  
Endogenous Retroviruses ◽  
Mass Spectrometry Data ◽  
Mutational Load ◽  
W Chromosome ◽  
Haldane’S Rule ◽  
Haldane's Rule ◽  
Genome Wide ◽  
Female Specific

It is a broadly observed pattern that the non-recombining regions of sex-limited chromosomes (Y and W) accumulate more repeats than the rest of the genome, even in species like birds with a low genome-wide repeat content. Here, we show that in birds with highly heteromorphic sex chromosomes, the W chromosome has a transposable element (TE) density of greater than 55% compared to the genome-wide density of less than 10%, and contains over half of all full-length (thus potentially active) endogenous retroviruses (ERVs) of the entire genome. Using RNA-seq and protein mass spectrometry data, we were able to detect signatures of female-specific ERV expression. We hypothesize that the avian W chromosome acts as a refugium for active ERVs, probably leading to female-biased mutational load that may influence female physiology similar to the ‘toxic-Y’ effect in Drosophila males. Furthermore, Haldane's rule predicts that the heterogametic sex has reduced fertility in hybrids. We propose that the excess of W-linked active ERVs over the rest of the genome may be an additional explanatory variable for Haldane's rule, with consequences for genetic incompatibilities between species through TE/repressor mismatches in hybrids. Together, our results suggest that the sequence content of female-specific W chromosomes can have effects far beyond sex determination and gene dosage. 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)’.

scholarly journals The avian W chromosome is a refugium for endogenous retroviruses with likely effects on female-biased mutational load and genetic incompatibilities

2020 ◽  
Author(s):  
Valentina Peona ◽  
Octavio M. Palacios-Gimenez ◽  
Julie Blommaert ◽  
Jing Liu ◽  
Tri Haryoko ◽  
...  
Keyword(s):  
Gene Dosage ◽  
Endogenous Retroviruses ◽  
Mass Spectrometry Data ◽  
Mutational Load ◽  
W Chromosome ◽  
Entire Genome ◽  
Haldane’S Rule ◽  
Haldane's Rule ◽  
Genome Wide ◽  
Female Specific

SummaryIt is a broadly observed pattern that the non-recombining regions of sex-limited chromosomes (Y and W) accumulate more repeats than the rest of the genome, even in species like birds with a low genome-wide repeat content. Here we show that in birds with highly heteromorphic sex chromosomes, the W chromosome has a transposable element (TE) density of >55% compared to the genome-wide density of <10%, and contains over half of all full-length (thus potentially active) endogenous retroviruses (ERVs) of the entire genome. Using RNA-seq and protein mass spectrometry data, we were able to detect signatures of female-specific ERV expression. We hypothesise that the avian W chromosome acts as a refugium for active ERVs, likely leading to female-biased mutational load that may influence female physiology similar to the “toxic-Y” effect in Drosophila. Furthermore, Haldane’s rule predicts that the heterogametic sex has reduced fertility in hybrids. We propose that the excess of W-linked active ERVs over the rest of the genome may be an additional explanatory variable for Haldane’s rule, with consequences for genetic incompatibilities between species through TE/repressor mismatches in hybrids. Together, our results suggest that the sequence content of female-specific W chromosomes can have effects far beyond sex determination and gene dosage.

scholarly journals Restricted X chromosome introgression and support for Haldane's rule in hybridizing damselflies

2021 ◽  
Author(s):  
Janne Swaegers ◽  
Rosa Ana Sanchez-Guillen ◽  
Pallavi Chauhan ◽  
Maren Wellenreuther ◽  
Bengt Hansson
Keyword(s):  
X Chromosome ◽  
Sex Chromosomes ◽  
Hybrid Zones ◽  
Haldane’S Rule ◽  
Haldane's Rule ◽  
Genome Wide ◽  
Determination System ◽  
Heterogametic Sex ◽  
Sex Determination System ◽  
Genomic Introgression

Contemporary hybrid zones act as natural laboratories for the investigation of species boundaries and allow to shed light on the little understood roles of sex chromosomes in species divergence. Sex chromosomes are considered to function as a hotspot of genetic divergence between species; indicated by less genomic introgression compared to autosomes during hybridisation. Moreover, they are thought to contribute to Haldane's rule which states that hybrids of the heterogametic sex are more likely to be inviable or sterile. To test these hypotheses, we used contemporary hybrid zones of Ischnura elegans, a damselfly species that has been expanding its range into the northern and western regions of Spain, leading to chronic hybridization with its sister species Ischnura graellsii. We analysed genome-wide SNPs in the Spanish I. elegans and I. graellsii hybrid zone and found (i) that the X chromosome shows less genomic introgression compared to autosomes and (ii) that males are underrepresented among admixed individuals as predicted by Haldane's rule. This is the first study in Odonata that suggests a role of the X chromosome in reproductive isolation. Moreover, our data adds to the few studies on species with X0 sex determination system and contradicts the hypothesis that the absence of a Y chromosome causes exceptions to Haldane's rule.

scholarly journals Genome-wide association mapping uncovers sex-associated copy number variation markers and female hemizygous regions on the W chromosome in Salix viminalis

BMC Genomics ◽  
2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Henrik R. Hallingbäck ◽  
Pascal Pucholt ◽  
Pär K. Ingvarsson ◽  
Ann Christin Rönnberg-Wästljung ◽  
Sofia Berlin
Keyword(s):  
Sex Determination ◽  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Chromosome 9 ◽  
Genome Wide Association ◽  
Salix Viminalis ◽  
Chromosome 15 ◽  
W Chromosome ◽  
Genome Wide ◽  
Heterogametic Sex

Abstract Background Sex chromosomes are in some species largely undifferentiated (homomorphic) with restricted sex determination regions. Homomorphic but different sex chromosomes are found in the closely related genera Populus and Salix indicating flexible sex determination systems, ideal for studies of processes involved in sex chromosome evolution. We have performed genome-wide association studies of sex and analysed sex chromosomes in a population of 265 wild collected Salix viminalis accessions and studied the sex determining locus. Results A total of 19,592 markers were used in association analyses using both Fisher’s exact tests and a single-marker mixed linear model, which resulted in 48 and 41 sex-associated (SA) markers respectively. Across all 48 SA markers, females were much more often heterozygous than males, which is expected if females were the heterogametic sex. The majority of the SA markers were, based on positions in the S. purpurea genome, located on chromosome 15, previously demonstrated to be the sex chromosome. Interestingly, when mapping the genotyping-by-sequencing sequence tag harbouring the two SA markers with the highest significance to the S. viminalis genomic scaffolds, five regions of very high similarity were found: three on a scaffold that represents a part of chromosome 15, one on a scaffold that represents a part of chromosome 9 and one on a scaffold not anchored to the genome. Based on segregation differences of the alleles at the two marker positions and on differences in PCR amplification between females and males we conclude that females had multiple copies of this DNA fragment (chromosome 9 and 15), whereas males only had one (chromosome 9). We therefore postulate that the female specific sequences have been copied from chromosome 9 and inserted on chromosome 15, subsequently developing into a hemizygous W chromosome linked region. Conclusions Our results support that sex determination in S. viminalis is controlled by one locus on chromosome 15. The segregation patterns observed at the SA markers furthermore confirm that S. viminalis females are the heterogametic sex. We also identified a translocation from chromosome 9 to the W chromosome.

scholarly journals Phylogeny, transposable element and sex chromosome evolution of the basal lineage of birds

2019 ◽  
Author(s):  
Zongji Wang ◽  
Jilin Zhang ◽  
Xiaoman Xu ◽  
Christopher Witt ◽  
Yuan Deng ◽  
...  
Keyword(s):  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Sequence Divergence ◽  
South American ◽  
Sex Chromosome Evolution ◽  
Rapid Speciation ◽  
Genome Wide ◽  
Divergence Pattern ◽  
Female Specific

AbstractSex chromosomes of mammals and most birds are heteromorphic, while those of many paleognaths (ratites and tinamous) are inexplicably homomorphic. To dissect the mechanisms underlying the different tempo of sex chromosome evolution, we produced high-quality genomes of 12 paleognathous species, and reconstructed their phylogeny based on alignments of the non-coding sequences extending to nearly 40% of the genome. Our phylogenomic tree grouped the South American rheas and tinamous together, and supported the independent evolution of gigantism and loss of flight among ratites. The small-bodied tinamous have much higher rates of genome-wide substitutions and transposon turnovers. Yet majorities of both have retained exceptionally long recombining regions occupying over half of the entire sex chromosome, with the rest sex-linked regions diverging from each other at a much lower rate relative to neognathous birds. Each species exhibits a punctuated sequence divergence pattern between sex chromosomes termed ‘evolutionary strata’, because of stepwise suppression of recombination. We concluded that all paleognaths share one evolutionary stratum with all other birds, and convergently formed between one to three strata after their rapid speciation. Contrary to the classic notion, we provided clear evidence that the youngest stratum of some tinamous formed without chromosomal inversion. Intriguingly, some of the encompassing W-linked genes have upregulated their expression levels in ovary, probably due to the female-specific selection. We proposed here that the unique male-only parental care system of paleognaths has reduced the intensity of sexual selection, and contributed to these species’ low rates of sex chromosome evolution. We also provided novel insights into the evolution of W-linked genes at their early stages.

scholarly journals Causes of sex ratio bias may account for unisexual sterility in hybrids: a new explanation of Haldane's rule and related phenomena.

Genetics ◽  
1991 ◽  
Vol 128 (4) ◽  
pp. 841-858 ◽  
Author(s):  
L D Hurst ◽  
A Pomiankowski
Keyword(s):  
Sex Ratio ◽  
Sex Chromosome ◽  
Meiotic Drive ◽  
Maternal Transmission ◽  
Haldane’S Rule ◽  
Haldane's Rule ◽  
Sex Ratio Bias ◽  
Y Chromosomes ◽  
Heterogametic Sex ◽  
Hybrid Cross

Abstract Unisexual hybrid disruption can be accounted for by interactions between sex ratio distorters which have diverged in the species of the hybrid cross. One class of unisexual hybrid disruption is described by Haldane's rule, namely that the sex which is absent, inviable or sterile is the heterogametic sex. This effect is mainly due to incompatibility between X and Y chromosomes. We propose that this incompatibility is due to a mutual imbalance between meiotic drive genes, which are more likely to evolve on sex chromosomes than autosomes. The incidences of taxa with sex chromosome drive closely matches those where Haldane's rule applies: Aves, Mammalia, Lepidoptera and Diptera. We predict that Haldane's rule is not universal but is correct for taxa with sex chromosome meiotic drive. A second class of hybrid disruption affects the male of the species regardless of which sex is heterogametic. Typically the genes responsible for this form of disruption are cytoplasmic. These instances are accounted for by the release from suppression of cytoplasmic sex ratio distorters when in a novel nuclear cytotype. Due to the exclusively maternal transmission of cytoplasm, cytoplasmic sex ratio distorters cause only female-biased sex ratios. This asymmetry explains why hybrid disruption is limited to the male.

SEX CHROMOSOME TRANSLOCATIONS IN THE EVOLUTION OF REPRODUCTIVE ISOLATION

Genetics ◽  
1972 ◽  
Vol 72 (2) ◽  
pp. 317-333
Author(s):  
Martin L Tracey
Keyword(s):  
Reproductive Isolation ◽  
X Chromosome ◽  
Sex Chromosome ◽  
Hybrid Sterility ◽  
Fixation Probability ◽  
Chromosomal Imbalance ◽  
Haldane’S Rule ◽  
Chromosome Translocations ◽  
Haldane's Rule ◽  
Heterogametic Sex

ABSTRACT Haldane's rule states that in organisms with differentiated sex chromosomes, hybrid sterility or inviability is generally expressed more frequently in the heterogametic sex. This observation has been variously explained as due to either genic or chromosomal imbalance. The fixation probabilities and mean times to fixation of sex-chromosome translocations of the type necessary to explain Haldane's rule on the basis of chromosomal imbalance have been estimated in small populations of Drosophila melanogaster. The fixation probability of an X chromosome carrying the long arm of the Y(X.YL) is approximately 30% greater than expected under the assumption of no selection. No fitness differences associated with the attached YL segment were detected. The fixation probability of a deficient Y chromosome is 300% greater than expected when the X chromosome contains the deleted portion of the Y. It is suggested that sex-chromosome translocations may play a role in the establishment of reproductive isolation.

Polymorphic minisatellite amplified on avian W chromosome

Genome ◽  
1991 ◽  
Vol 34 (3) ◽  
pp. 489-493 ◽  
Author(s):  
Patricia P. Rabenold ◽  
Walter H. Piper ◽  
Mark D. Decker ◽  
Dennis J. Minchella
Keyword(s):  
Molecular Weight ◽  
Sex Chromosome ◽  
Large Female ◽  
W Chromosome ◽  
Total Molecular Weight ◽  
Specific Fragment ◽  
Female Specific ◽  
Hypervariable Loci ◽  
Pairing Region ◽  
Campylorhynchus Nuchalis

Jeffrey's minisatellite probe 33.15, which screens dozens of hypervariable loci throughout the genome, detects female-specific fragments in stripe-backed wrens (Campylorhynchus nuchalis). HaeIII subdivides the single large female-specific fragment observed with other enzymes into a polymorphic suite of fragments of similar total molecular weight among patterns. Sex-linked HaeIII haplotypes are perfectly transmitted from mother to daughter but not to sons. These results suggest that the female-specific HaeIII fragments represent variable subunits of a single long tandem repetitive array composed of approximately 20-bp repetitive units located outside the pairing region of the W chromosome. That sex-linked fragments do not occur in the congener Campylorhynchus griseus suggests that their entrapment and amplification on the W chromosome in C. nuchalis occurred since the divergence of the two species.Key words: minisatellites, sex chromosome, W chromosome, amplification.

scholarly journals Lack of intrinsic postzygotic isolation in haplodiploid male hybrids despite high genetic distance

2020 ◽  
Author(s):  
Emily E. Bendall ◽  
Kayla M. Mattingly ◽  
Amanda J. Moehring ◽  
Catherine R. Linnen
Keyword(s):  
Genetic Distance ◽  
Genetic Divergence ◽  
Sex Chromosome ◽  
Postzygotic Isolation ◽  
Entire Genome ◽  
Male And Female ◽  
Haldane’S Rule ◽  
Haldane's Rule ◽  
Heterogametic Sex ◽  
High Genetic Distance

AbstractEvolutionary biologists have long been interested in understanding the mechanisms underlying Haldane’s rule. The explanatory theories of dominance and faster-X, which are based on recessive alleles being expressed in the heterogametic sex, have been proposed as common mechanisms. These mechanisms predict that greater hemizygosity leads to both faster evolution and greater expression of intrinsic postzygotic isolation. Under these mechanisms, haplodiploids should evolve and express intrinsic postzygotic isolation faster than diploids because the entire genome is analogous to a sex chromosome. Here, we measure sterility and inviability in hybrids between Neodiprion pinetum and N. lecontei, a pair of haplodiplopids that differ morphologically, behaviorally, and genetically. We compare the observed isolation to that expected from published estimates of isolation in diploids at comparable levels of genetic divergence. We find that both male and female hybrids are viable and fertile, which is less isolation than expected. We then discuss several potential explanations for this surprising lack of isolation, including alternative mechanisms for Haldane’s rule and a frequently overlooked quirk of haplodiploid genetics that may slow the emergence of complete intrinsic postzygotic isolation in hybrid males. Finally, we describe how haplodiploids, an underutilized resource, can be used to differentiate between mechanisms of Haldane’s rule.

scholarly journals Complex basis of hybrid female sterility and Haldane's rule in Heliconius butterflies: Z-linkage and epistasis

2021 ◽  
Author(s):  
Neil Rosser ◽  
Nathaniel B. Edelman ◽  
Lucie Queste ◽  
Michaela Nelson ◽  
Fernando A. Seixas ◽  
...  
Keyword(s):  
Sex Chromosome ◽  
Hybrid Sterility ◽  
Differentially Expressed ◽  
F1 Hybrids ◽  
Female Sterility ◽  
Ovary Development ◽  
Z Chromosome ◽  
Hybrid Female ◽  
Haldane’S Rule ◽  
Haldane's Rule

Hybrids between diverging populations are often sterile or inviable. Hybrid unfitness usually evolves first in the heterogametic sex -- a pattern known as Haldane's rule. The genetics of Haldane's Rule have been extensively studied in species where the male is the heterogametic (XX/XY) sex, but its basis in taxa where the female is heterogametic (ZW/ZZ), such as Lepidoptera and birds, is largely unknown. Here, we analyse a new case of female hybrid sterility between geographic subspecies of Heliconius pardalinus. The two subspecies mate freely in captivity, but female F1 hybrids in both directions of cross are sterile. Sterility is due to arrested development of oocytes after they become differentiated from nurse cells, but before yolk deposition. We backcrossed fertile male F1 hybrids to parental females, and mapped quantitative trait loci (QTLs) for female sterility. We also identified genes differentially expressed in the ovary, and as a function of oocyte development. The Z chromosome has a major effect, similar to the "large X effect" in Drosophila, with strong epistatic interactions between loci at either end of the Z chromosome, and between the Z chromosome and autosomal loci on chromosomes 8 and 20. Among loci differentially expressed between females with arrested vs. non-arrested ovary development, we identified six candidate genes known also from Drosophila melanogaster and Parage aegeria oogenesis. This study is the first to characterize hybrid sterility using genome mapping in the Lepidoptera. We demonstrate that sterility is produced by multiple complex epistastic interactions often involving the sex chromosome, as predicted by the dominance theory of Haldane's Rule.

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