scholarly journals Divergence and Remarkable Diversity of the Y Chromosome in Guppies

Author(s):  
Pedro Almeida ◽  
Benjamin A Sandkam ◽  
Jake Morris ◽  
Iulia Darolti ◽  
Felix Breden ◽  
...  

Abstract The guppy sex chromosomes show an extraordinary diversity in divergence across populations and closely related species. In order to understand the dynamics of the guppy Y chromosome, we used linked-read sequencing to assess Y chromosome evolution and diversity across upstream and downstream population pairs that vary in predator and food abundance in three replicate watersheds. Based on our population-specific genome assemblies, we first confirmed and extended earlier reports of two strata on the guppy sex chromosomes. Stratum I shows significant accumulation of male-specific sequence, consistent with Y divergence, and predates the colonization of Trinidad. In contrast, Stratum II shows divergence from the X, but no Y-specific sequence, and this divergence is greater in three replicate upstream populations compared with their downstream pair. Despite longstanding assumptions that sex chromosome recombination suppression is achieved through inversions, we find no evidence of inversions associated with either Stratum I or Stratum II. Instead, we observe a remarkable diversity in Y chromosome haplotypes within each population, even in the ancestral Stratum I. This diversity is likely due to gradual mechanisms of recombination suppression, which, unlike an inversion, allow for the maintenance of multiple haplotypes. In addition, we show that this Y diversity is dominated by low-frequency haplotypes segregating in the population, suggesting a link between haplotype diversity and female preference for rare Y-linked color variation. Our results reveal the complex interplay between recombination suppression and Y chromosome divergence at the earliest stages of sex chromosome divergence.

Author(s):  
Pedro Almeida ◽  
Benjamin A. Sandkam ◽  
Jake Morris ◽  
Iulia Darolti ◽  
Felix Breden ◽  
...  

AbstractThe guppy sex chromosomes show an extraordinary diversity in divergence across populations and closely related species. In order to understand the dynamics of the guppy Y chromosome, we used linked-read sequencing to assess Y chromosome evolution and diversity across upstream and downstream population pairs that vary in predator and food abundance in three replicate watersheds. Based on our population-specific genome assemblies, we first confirmed and extended earlier reports of two strata on the guppy sex chromosomes. Stratum I shows significant accumulation of male-specific sequence, consistent with Y divergence, and predates the colonization of Trinidad. In contrast, Stratum II shows divergence from the X, but no Y-specific sequence, and this divergence is greater in three replicate upstream populations compared to their downstream pair. Despite longstanding assumptions that sex chromosome recombination suppression is achieved through inversions, we find no evidence of inversions associated with either Stratum I or Stratum II. Instead, we observe a remarkable diversity in Y chromosome haplotypes within each population, even in the ancestral Stratum I. This diversity is likely due to gradual mechanisms of recombination suppression, which, unlike an inversion, allow for the maintenance of multiple haplotypes. In addition, we show that this Y diversity is dominated by low-frequency haplotypes segregating in the population, suggesting a link between haplotype diversity and female-preference for rare Y-linked colour variation. Our results reveal the complex interplay between recombination suppression and Y chromosome divergence at the earliest stages of sex chromosome divergence.


2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Lingzhan Xue ◽  
Yu Gao ◽  
Meiying Wu ◽  
Tian Tian ◽  
Haiping Fan ◽  
...  

Abstract Background The origin of sex chromosomes requires the establishment of recombination suppression between the proto-sex chromosomes. In many fish species, the sex chromosome pair is homomorphic with a recent origin, providing species for studying how and why recombination suppression evolved in the initial stages of sex chromosome differentiation, but this requires accurate sequence assembly of the X and Y (or Z and W) chromosomes, which may be difficult if they are recently diverged. Results Here we produce a haplotype-resolved genome assembly of zig-zag eel (Mastacembelus armatus), an aquaculture fish, at the chromosomal scale. The diploid assembly is nearly gap-free, and in most chromosomes, we resolve the centromeric and subtelomeric heterochromatic sequences. In particular, the Y chromosome, including its highly repetitive short arm, has zero gaps. Using resequencing data, we identify a ~7 Mb fully sex-linked region (SLR), spanning the sex chromosome centromere and almost entirely embedded in the pericentromeric heterochromatin. The SLRs on the X and Y chromosomes are almost identical in sequence and gene content, but both are repetitive and heterochromatic, consistent with zero or low recombination. We further identify an HMG-domain containing gene HMGN6 in the SLR as a candidate sex-determining gene that is expressed at the onset of testis development. Conclusions Our study supports the idea that preexisting regions of low recombination, such as pericentromeric regions, can give rise to SLR in the absence of structural variations between the proto-sex chromosomes.


PLoS Genetics ◽  
2020 ◽  
Vol 16 (11) ◽  
pp. e1009121
Author(s):  
Benjamin L. S. Furman ◽  
Caroline M. S. Cauret ◽  
Martin Knytl ◽  
Xue-Ying Song ◽  
Tharindu Premachandra ◽  
...  

In many species, sexual differentiation is a vital prelude to reproduction, and disruption of this process can have severe fitness effects, including sterility. It is thus interesting that genetic systems governing sexual differentiation vary among—and even within—species. To understand these systems more, we investigated a rare example of a frog with three sex chromosomes: the Western clawed frog, Xenopus tropicalis. We demonstrate that natural populations from the western and eastern edges of Ghana have a young Y chromosome, and that a male-determining factor on this Y chromosome is in a very similar genomic location as a previously known female-determining factor on the W chromosome. Nucleotide polymorphism of expressed transcripts suggests genetic degeneration on the W chromosome, emergence of a new Y chromosome from an ancestral Z chromosome, and natural co-mingling of the W, Z, and Y chromosomes in the same population. Compared to the rest of the genome, a small sex-associated portion of the sex chromosomes has a 50-fold enrichment of transcripts with male-biased expression during early gonadal differentiation. Additionally, X. tropicalis has sex-differences in the rates and genomic locations of recombination events during gametogenesis that are similar to at least two other Xenopus species, which suggests that sex differences in recombination are genus-wide. These findings are consistent with theoretical expectations associated with recombination suppression on sex chromosomes, demonstrate that several characteristics of old and established sex chromosomes (e.g., nucleotide divergence, sex biased expression) can arise well before sex chromosomes become cytogenetically distinguished, and show how these characteristics can have lingering consequences that are carried forward through sex chromosome turnovers.


2020 ◽  
Vol 12 (6) ◽  
pp. 965-977 ◽  
Author(s):  
Iulia Darolti ◽  
Alison E Wright ◽  
Judith E Mank

Abstract The loss of recombination triggers divergence between the sex chromosomes and promotes degeneration of the sex-limited chromosome. Several livebearers within the genus Poecilia share a male-heterogametic sex chromosome system that is roughly 20 Myr old, with extreme variation in the degree of Y chromosome divergence. In Poecilia picta, the Y is highly degenerate and associated with complete X chromosome dosage compensation. In contrast, although recombination is restricted across almost the entire length of the sex chromosomes in Poecilia reticulata and Poecilia wingei, divergence between the X chromosome and the Y chromosome is very low. This clade therefore offers a unique opportunity to study the forces that accelerate or hinder sex chromosome divergence. We used RNA-seq data from multiple families of both P. reticulata and P. wingei, the species with low levels of sex chromosome divergence, to differentiate X and Y coding sequences based on sex-limited SNP inheritance. Phylogenetic tree analyses reveal that occasional recombination has persisted between the sex chromosomes for much of their length, as X- and Y-linked sequences cluster by species instead of by gametolog. This incomplete recombination suppression maintains the extensive homomorphy observed in these systems. In addition, we see differences between the previously identified strata in the phylogenetic clustering of X–Y orthologs, with those that cluster by chromosome located in the older stratum, the region previously associated with the sex-determining locus. However, recombination arrest appears to have expanded throughout the sex chromosomes more gradually instead of through a stepwise process associated with inversions.


BMC Genomics ◽  
2020 ◽  
Vol 21 (1) ◽  
Author(s):  
Duminda Sampath Bandara Dissanayake ◽  
Clare Ellen Holleley ◽  
Laura Kate Hill ◽  
Denis O’Meally ◽  
Janine Eileen Deakin ◽  
...  

Abstract Background Homologous sex chromosomes can differentiate over time because recombination is suppressed in the region of the sex determining locus, leading to the accumulation of repeats, progressive loss of genes that lack differential influence on the sexes and sequence divergence on the hemizygous homolog. Divergence in the non-recombining regions leads to the accumulation of Y or W specific sequence useful for developing sex-linked markers. Here we use in silico whole-genome subtraction to identify putative sex-linked sequences in the scincid lizard Bassiana duperreyi which has heteromorphic XY sex chromosomes. Results We generated 96.7 × 109 150 bp paired-end genomic sequence reads from a XY male and 81.4 × 109 paired-end reads from an XX female for in silico whole genome subtraction to yield Y enriched contigs. We identified 7 reliable markers which were validated as Y chromosome specific by polymerase chain reaction (PCR) against a panel of 20 males and 20 females. Conclusions The sex of B. duperreyi can be reversed by low temperatures (XX genotype reversed to a male phenotype). We have developed sex-specific markers to identify the underlying genotypic sex and its concordance or discordance with phenotypic sex in wild populations of B. duperreyi. Our pipeline can be applied to isolate Y or W chromosome-specific sequences of any organism and is not restricted to sequence residing within single-copy genes. This study greatly improves our knowledge of the Y chromosome in B. duperreyi and will enhance future studies of reptile sex determination and sex chromosome evolution.


2021 ◽  
Vol 12 ◽  
Author(s):  
Maria F. Torres ◽  
Yasmin A. Mohamoud ◽  
Shameem Younuskunju ◽  
Karsten Suhre ◽  
Joel A. Malek

The genus Phoenix includes the fruit producing date palm tree among 14 species that are all dioecious. Females produce the fruit that are high in sugar content and used in multiple countries ranging from North Africa to South Asia, especially from the Phoenix dactylifera, Phoenix sylvestris, and Phoenix canariensis species. While females produce the fruit, understanding of the genetic basis of sex control only began recently. Through genus-wide sequencing of males and females we recently identified three genes that are conserved in all males and absent in all females of the genus and confirmed an XY sex chromosome system. While our previous study focused on conservation of male-specific sequences at the genus-level, it would be of interest to better understand the spread of male-specific sequences away from the core conserved male genes on the Y chromosome during speciation. To this end, we enumerated male-specific 16 bp sequences using three male/female pairs from the western subpopulation of date palm and documented the density of these sequences in contigs of a phased date palm genome assembly. Here we show that male specific sequences in the date palm Y chromosome have likely spread in defined events that appear as blocks of varying density with significant changes in density between them. Collinearity of genes in these blocks with oil palm shows high synteny with chromosome 10 between megabase 15 and 23 and reveals that large sections of the date palm Y chromosome have maintained the ancestral structure even as recombination has stopped between X and Y.


2020 ◽  
Vol 117 (39) ◽  
pp. 24359-24368
Author(s):  
Nima Rafati ◽  
Junfeng Chen ◽  
Amaury Herpin ◽  
Mats E. Pettersson ◽  
Fan Han ◽  
...  

The mechanisms underlying sex determination are astonishingly plastic. Particularly the triggers for the molecular machinery, which recalls either the male or female developmental program, are highly variable and have evolved independently and repeatedly. Fish show a huge variety of sex determination systems, including both genetic and environmental triggers. The advent of sex chromosomes is assumed to stabilize genetic sex determination. However, because sex chromosomes are notoriously cluttered with repetitive DNA and pseudogenes, the study of their evolution is hampered. Here we reconstruct the birth of a Y chromosome present in the Atlantic herring. The region is tiny (230 kb) and contains only three intact genes. The candidate male-determining gene BMPR1BBY encodes a truncated form of a BMP1B receptor, which originated by gene duplication and translocation and underwent rapid protein evolution. BMPR1BBY phosphorylates SMADs in the absence of ligand and thus has the potential to induce testis formation. The Y region also contains two genes encoding subunits of the sperm-specific Ca2+ channel CatSper required for male fertility. The herring Y chromosome conforms with a characteristic feature of many sex chromosomes, namely, suppressed recombination between a sex-determining factor and genes that are beneficial for the given sex. However, the herring Y differs from other sex chromosomes in that suppression of recombination is restricted to an ∼500-kb region harboring the male-specific and sex-associated regions. As a consequence, any degeneration on the herring Y chromosome is restricted to those genes located in the small region affected by suppressed recombination.


2020 ◽  
Author(s):  
Duminda Sampath Bandara Dissanayake ◽  
Clare Ellen Holleley ◽  
Laura Kate Hill ◽  
Denis O’Meally ◽  
Janine Eileen Deakin ◽  
...  

Abstract Background: Homologous sex chromosomes can differentiate over time because recombination is suppressed in the region of the sex determining locus, leading to the accumulation of repeats, progressive loss of genes that lack differential influence on the sexes and sequence divergence on the hemizygous homolog. Divergence in the non-recombining regions leads to the accumulation of Y or W specific sequence useful for developing sex-linked markers. Here we use in silico whole-genome subtraction to identify putative sex-linked sequences in the scincid lizard Bassiana duperreyi which has heteromorphic XY sex chromosomes. Results: We generated 96.7 x 10 9 150 bp paired-end genomic sequence reads from a XY male and 81.4 x 10 9 paired-end reads from an XX female for in silico whole genome subtraction to yield Y enriched contigs. We identified 7 reliable markers which were validated as Y chromosome specific by polymerase chain reaction (PCR) against a panel of 20 males and 20 females. Conclusions: The sex of B. duperreyi can be reversed by low temperatures (XX genotype reversed to a male phenotype). We have developed sex-specific markers to identify the underlying genotypic sex and its concordance or discordance with phenotypic sex in wild populations of B. duperreyi . Our pipeline can be applied to isolate Y or W chromosome-specific sequences of any organism and is not restricted to sequence residing within single-copy genes. This study greatly improves our knowledge of the Y chromosome in B. duperreyi and will enhance future studies of reptile sex determination and sex chromosome evolution.


2020 ◽  
Author(s):  
Duminda S.B. Dissanayake ◽  
Clare Holleley ◽  
Laura Hill ◽  
D. O’Meally ◽  
J. Deakin ◽  
...  

Abstract Background: Homologous sex chromosomes can differentiate over time because recombination is suppressed in the region of the sex determining locus, leading to the accumulation of repeats, progressive loss of genes that lack differential influence on the sexes and sequence divergence on the heterozygous homolog. Divergence in the non-recombining regions leads to the accumulation of Y or W specific sequence useful for developing sex-linked markers. Here we use in-silico whole-genome subtraction to identify putative sex-linked sequences in the scincid lizard Bassiana duperreyi which has heteromorphic XY sex chromosomes. Results: We generated 96.7 x 109 150bp paired-end genomic sequence reads from a XY male and 81.4 x 109 paired-end reads from an XX female for in-silico whole genome subtraction to yield Y enriched contigs. We identified 7 reliable markers which were validated as XY male-specific by polymerase chain reaction (PCR) against a panel of 20 males and 20 females. Conclusions: The sex of B. duperreyi can be reversed by low temperatures (XX genotype reversed to a male phenotype). We have developed sex-specific markers to identify the underlying genotypic sex and its concordance or discordance with phenotypic sex in wild populations of B. duperreyi. Our pipeline can be applied to isolate Y or W chromosome-specific sequences of any organism and is not restricted to sequence residing within single-copy genes. This study greatly improves our knowledge of the Y chromosome in B. duperreyi and will enhance future studies of reptile sex determination and sex chromosome evolution.


2020 ◽  
Author(s):  
Duminda Sampath Bandara Dissanayake ◽  
Clare Ellen Holleley ◽  
Laura Kate Hill ◽  
Denis O’Meally ◽  
Janine Eileen Deakin ◽  
...  

Abstract Background: Homologous sex chromosomes can differentiate over time because recombination is suppressed in the region of the sex determining locus, leading to the accumulation of repeats, progressive loss of genes that lack differential influence on the sexes and sequence divergence on the hemizygous homolog. Divergence in the non-recombining regions leads to the accumulation of Y or W specific sequence useful for developing sex-linked markers. Here we use in silico whole-genome subtraction to identify putative sex-linked sequences in the scincid lizard Bassiana duperreyi which has heteromorphic XY sex chromosomes. Results: We generated 96.7 x 109 150 bp paired-end genomic sequence reads from a XY male and 81.4 x 109 paired-end reads from an XX female for in silico whole genome subtraction to yield Y enriched contigs. We identified 7 reliable markers which were validated as Y chromosome specific by polymerase chain reaction (PCR) against a panel of 20 males and 20 females. Conclusions: The sex of B. duperreyi can be reversed by low temperatures (XX genotype reversed to a male phenotype). We have developed sex-specific markers to identify the underlying genotypic sex and its concordance or discordance with phenotypic sex in wild populations of B. duperreyi. Our pipeline can be applied to isolate Y or W chromosome-specific sequences of any organism and is not restricted to sequence residing within single-copy genes. This study greatly improves our knowledge of the Y chromosome in B. duperreyi and will enhance future studies of reptile sex determination and sex chromosome evolution.


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