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

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.

2018 ◽  
Vol 40 (1) ◽  
pp. 114-131 ◽  
Author(s):  
Liliana Cortés-Ortiz ◽  
Marcella D. Nidiffer ◽  
Javier Hermida-Lagunes ◽  
Francisco García-Orduña ◽  
Ariadna Rangel-Negrín ◽  
...  

2019 ◽  
Author(s):  
Anastasia N. Naumenko ◽  
Dmitriy A. Karagodin ◽  
Andrey A. Yurchenko ◽  
Anton V. Moskaev ◽  
Olga I. Martin ◽  
...  

Abstract Background A dominant malaria vector, Anopheles messeae, is a highly polymorphic species with wide distribution throughout Eurasia. Five highly polymorphic inversions associated with the geographical distribution of the species have been reported. A sister species, An. daciae, was described and discriminated from An. messeae based on five fixed nucleotide substitutions in the internal transcribed spacer 2 (ITS2) of ribosomal DNA. However, the levels of genomic divergence, chromosomal variation, and ecological differentiation between these two cryptic species remain unexplored. Results In this study, we sequenced ITS2 and analyzed the inversion frequencies of 289 Anopheles larvae specimens collected from three locations in the Moscow region. We identified a high abundance of both An. messeae and An. daciae in all three locations. Five individual genomes for each species of An. messeae and An. daciae from one location were sequenced. Our study confirmed five previously described nucleotide substitutions in the ITS2 of An. messeae. However, we found that the ITS2 sequence in An. daciae was heterogenic in three of the five positions. Fixed nucleotide differences between An. messeae and An. daciae were found only in the last two positions. One mosquito was identified as a hybrid between An. messeae and An. daciae based on heterogeneous substitutions in all five positions. Although, the genomic sequence comparison demonstrated genome-wide divergence between the two species, which is especially pronounced on the X chromosome, an ADMIXTURE cluster analysis demonstrated the presence of two admixed individuals suggesting ongoing hybridization. Cytogenetic analysis demonstrated that An. messeae and An. daciae significantly differ from each other by their frequency of polymorphic inversions. Inversion X1 was fixed in An. messeae but was polymorphic in all An. daciae populations. The frequency of polymorphic autosomal inversions was higher in An. messeae than in An. daciae. The species composition was different among the studied locations suggesting species-specific ecological preferences. Conclusions Our study demonstrated that An. messeae and An. daciae represent closely related cryptic species with incomplete reproductive isolation that are able to maintain genomic differentiation in sympatry despite ongoing genetic introgression. The X chromosome plays an important role in the reproductive isolation between the species.


2017 ◽  
Vol 372 (1733) ◽  
pp. 20160363 ◽  
Author(s):  
Anna Sahakyan ◽  
Kathrin Plath ◽  
Claire Rougeulle

The human blastocyst forms 5 days after one of the smallest human cells (the sperm) fertilizes one of the largest human cells (the egg). Depending on the sex-chromosome contribution from the sperm, the resulting embryo will either be female, with two X chromosomes (XX), or male, with an X and a Y chromosome (XY). In early development, one of the major differences between XX female and XY male embryos is the conserved process of X-chromosome inactivation (XCI), which compensates gene expression of the two female X chromosomes to match the dosage of the single X chromosome of males. Most of our understanding of the pre-XCI state and XCI establishment is based on mouse studies, but recent evidence from human pre-implantation embryo research suggests that many of the molecular steps defined in the mouse are not conserved in human. Here, we will discuss recent advances in understanding the control of X-chromosome dosage compensation in early human embryonic development and compare it to that of the mouse. This article is part of the themed issue ‘X-chromosome inactivation: a tribute to Mary Lyon’.


Genome ◽  
1990 ◽  
Vol 33 (3) ◽  
pp. 340-347 ◽  
Author(s):  
R. Frankham

For X–Y exchange to be of importance in the coevolution of X and Y rDNA, there must be a mechanism to maintain cytologically normal X chromosomes in the face of continual infusions of X.YL chromosomes produced by X–Y exchanges. Replicated populations were founded with different frequencies of isogenic X and X.YL chromosomes. The X.YL chromosome declined in frequency over time in all lines. Relative fitnesses, estimated from chromosome frequency trajectories, were 0.40, 1.01, and 1.0 for X.YL/X.YL, X.YL/X, and X/X females and 0.75 and 1.0 for X.YL/Y and X/Y males, respectively. The equilibrium frequency for the X.YL chromosome due to the balance between X–Y exchange and selection was predicted to be 4–16 × 10−4. The results strengthen the evidence for the involvement of X–Y exchange in the coevolution of X and Y rDNA arrays. Conditions for the evolution of reproductive isolation by sex-chromosome translocation are much less probable than previously supposed since the X.YL translocation chromosome is at a selective disadvantage to cytologically normal X chromosomes. Additional heterochromatin was not neutral but was only deleterious beyond a threshold, as one dose of the heterochromatic XL arm did not reduce female reproductive fitness, but two doses did.Key words: Drosophila, rRNA, heterochromatin, fitness, speciation.


Genetics ◽  
1972 ◽  
Vol 72 (2) ◽  
pp. 317-333
Author(s):  
Martin L Tracey

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.


2018 ◽  
Vol 28 (6) ◽  
pp. 1246-1262 ◽  
Author(s):  
Daniel M. Hooper ◽  
Simon C. Griffith ◽  
Trevor D. Price

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Yisrael Rappaport ◽  
Hanna Achache ◽  
Roni Falk ◽  
Omer Murik ◽  
Oren Ram ◽  
...  

AbstractDuring meiosis, gene expression is silenced in aberrantly unsynapsed chromatin and in heterogametic sex chromosomes. Initiation of sex chromosome silencing is disrupted in meiocytes with sex chromosome-autosome translocations. To determine whether this is due to aberrant synapsis or loss of continuity of sex chromosomes, we engineered Caenorhabditis elegans nematodes with non-translocated, bisected X chromosomes. In early meiocytes of mutant males and hermaphrodites, X segments are enriched with euchromatin assembly markers and active RNA polymerase II staining, indicating active transcription. Analysis of RNA-seq data showed that genes from the X chromosome are upregulated in gonads of mutant worms. Contrary to previous models, which predicted that any unsynapsed chromatin is silenced during meiosis, our data indicate that unsynapsed X segments are transcribed. Therefore, our results suggest that sex chromosome chromatin has a unique character that facilitates its meiotic expression when its continuity is lost, regardless of whether or not it is synapsed.


2015 ◽  
Vol 7 (2) ◽  
pp. 636-641 ◽  
Author(s):  
Rebecca Dean ◽  
Fabian Zimmer ◽  
Judith E. Mank

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Ryoma Ota ◽  
Makoto Hayashi ◽  
Shumpei Morita ◽  
Hiroki Miura ◽  
Satoru Kobayashi

AbstractDosage compensation is a mechanism that equalizes sex chromosome gene expression between the sexes. In Drosophila, individuals with two X chromosomes (XX) become female, whereas males have one X chromosome (XY). In males, dosage compensation of the X chromosome in the soma is achieved by five proteins and two non-coding RNAs, which assemble into the male-specific lethal (MSL) complex to upregulate X-linked genes twofold. By contrast, it remains unclear whether dosage compensation occurs in the germline. To address this issue, we performed transcriptome analysis of male and female primordial germ cells (PGCs). We found that the expression levels of X-linked genes were approximately twofold higher in female PGCs than in male PGCs. Acetylation of lysine residue 16 on histone H4 (H4K16ac), which is catalyzed by the MSL complex, was undetectable in these cells. In male PGCs, hyperactivation of X-linked genes and H4K16ac were induced by overexpression of the essential components of the MSL complex, which were expressed at very low levels in PGCs. Together, these findings indicate that failure of MSL complex formation results in the absence of X-chromosome dosage compensation in male PGCs.


Oryx ◽  
2002 ◽  
Vol 36 (3) ◽  
pp. 266-271 ◽  
Author(s):  
Juan Carlos Serio-Silva ◽  
Victor Rico-Gray

We studied changes in germination rates and dispersal distance of seeds of Ficus perforata and F. lundelli dispersed by howler monkeys (Alouatta palliata mexicana), in a small (40 ha) ‘disturbed’ and a larger (>600 ha) ‘preserved’ tropical rainforest in southern Veracruz, Mexico. The interaction between A. p. mexicana and Ficus (Urostigma) spp. is beneficial for the interacting species and has important implications for their conservation. Howler monkeys gain from the ingestion of an important food source, germination rates of Ficus seeds are improved by passage through the monkeys' digestive tract, and the seeds are more likely to be deposited in a site suitable for germination and development. Seed dispersal distances are relatively larger in the preserved site, with both the size of the forest area and the spatial pattern of Ficus affecting the dispersal process. In a large forest fragment with ‘regularly’ distributed Ficus individuals the howler monkeys move away from the seed source, increasing the probability that the seeds are desposited on a tree other than Ficus, which is important for the germination and future development of a hemiepiphytic species. In a small forest fragment with trees distributed in clumps howlers repeatedly use the same individual trees, and faeces containing seeds may be dropped on unsuitable trees more often. These are key issues when addressing conservation policies for fragmented forests.


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