scholarly journals Exaggerated heterochiasmy in a fish with sex-linked male coloration polymorphisms

2019 ◽  
Vol 116 (14) ◽  
pp. 6924-6931 ◽  
Author(s):  
Roberta Bergero ◽  
Jim Gardner ◽  
Beth Bader ◽  
Lengxob Yong ◽  
Deborah Charlesworth
Keyword(s):  
Sex Chromosomes ◽  
Poecilia Reticulata ◽  
Low Frequency ◽  
Male Meiosis ◽  
Chromosome 12 ◽  
Sexually Dimorphic ◽  
Recombination Suppression ◽  
Physical Maps ◽  
Suppressed Recombination ◽  
Male Coloration

It is often stated that polymorphisms for mutations affecting fitness of males and females in opposite directions [sexually antagonistic (SA) polymorphisms] are the main selective force for the evolution of recombination suppression between sex chromosomes. However, empirical evidence to discriminate between different hypotheses is difficult to obtain. We report genetic mapping results in laboratory-raised families of the guppy (Poecilia reticulata), a sexually dimorphic fish with SA polymorphisms for male coloration genes, mostly on the sex chromosomes. Comparison of the genetic and physical maps shows that crossovers are distributed very differently in the two sexes (heterochiasmy); in male meiosis, they are restricted to the termini of all four chromosomes studied, including chromosome 12, which carries the sex-determining locus. Genome resequencing of male and female guppies from a population also indicates sex linkage of variants across almost the entire chromosome 12. More than 90% of the chromosome carrying the male-determining locus is therefore transmitted largely through the male lineage. A lack of heterochiasmy in a related fish species suggests that it originated recently in the lineage leading to the guppy. Our findings do not support the hypothesis that suppressed recombination evolved in response to the presence of SA polymorphisms. Instead, a low frequency of recombination on a chromosome that carries a male-determining locus and has not undergone genetic degeneration has probably facilitated the establishment of male-beneficial coloration polymorphisms.

scholarly journals Sexually dimorphic recombination can facilitate the establishment of sexually antagonistic polymorphisms in guppies

2018 ◽  
Author(s):  
Roberta Bergero ◽  
Jim Gardner ◽  
Beth Bader ◽  
Lengxob Yong ◽  
Deborah Charlesworth
Keyword(s):  
Sex Chromosomes ◽  
Poecilia Reticulata ◽  
Common Ancestor ◽  
Sex Chromosome ◽  
Empirical Support ◽  
Male Meiosis ◽  
Sexually Dimorphic ◽  
Sex Linkage ◽  
Recombination Suppression ◽  
Males And Females

Summary/AbstractRecombination suppression between sex chromosomes is often stated to evolve in response to polymorphisms for mutations that affect fitness of males and females in opposite directions (sexually antagonistic, or SA, mutations), but direct empirical support is lacking. The sex chromosomes of the fish Poecilia reticulata (the guppy) carry SA polymorphisms, making them excellent for testing this hypothesis for the evolution of sex linkage. We resequenced genomes of male and female guppies and, unexpectedly, found that variants on the sex chromosome indicate no extensive region with fully sex-linked genotypes, though many variants show strong evidence for partial sex linkage. We present genetic mapping results that help understand the evolution of the guppy sex chromosome pair. We find very different distributions of crossing over in the two sexes, with recombination events in male meiosis detected only at the tips of the chromosomes. The guppy may exemplify a route for sex chromosome evolution in which low recombination in males, likely evolved in a common ancestor, has facilitated the establishment of sexually antagonistic polymorphisms.

scholarly journals Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers

2019 ◽  
Vol 116 (38) ◽  
pp. 19031-19036 ◽  
Author(s):  
Iulia Darolti ◽  
Alison E. Wright ◽  
Benjamin A. Sandkam ◽  
Jake Morris ◽  
Natasha I. Bloch ◽  
...  
Keyword(s):  
Y Chromosome ◽  
Dosage Compensation ◽  
Sex Chromosomes ◽  
Poecilia Reticulata ◽  
Sex Chromosome ◽  
Sequencing Data ◽  
Chromosome Differentiation ◽  
Y Chromosomes ◽  
Shared Ancestry ◽  
Suppressed Recombination

Once recombination is halted between the X and Y chromosomes, sex chromosomes begin to differentiate and transition to heteromorphism. While there is a remarkable variation across clades in the degree of sex chromosome divergence, far less is known about the variation in sex chromosome differentiation within clades. Here, we combined whole-genome and transcriptome sequencing data to characterize the structure and conservation of sex chromosome systems across Poeciliidae, the livebearing clade that includes guppies. We found that the Poecilia reticulata XY system is much older than previously thought, being shared not only with its sister species, Poecilia wingei, but also with Poecilia picta, which diverged roughly 20 million years ago. Despite the shared ancestry, we uncovered an extreme heterogeneity across these species in the proportion of the sex chromosome with suppressed recombination, and the degree of Y chromosome decay. The sex chromosomes in P. reticulata and P. wingei are largely homomorphic, with recombination in the former persisting over a substantial fraction. However, the sex chromosomes in P. picta are completely nonrecombining and strikingly heteromorphic. Remarkably, the profound degradation of the ancestral Y chromosome in P. picta is counterbalanced by the evolution of functional chromosome-wide dosage compensation in this species, which has not been previously observed in teleost fish. Our results offer important insight into the initial stages of sex chromosome evolution and dosage compensation.

scholarly journals Evolution of the canonical sex chromosomes of the guppy and its relatives

2021 ◽  
Author(s):  
Mark Kirkpatrick ◽  
Jason M Sardell ◽  
Brendan J Pinto ◽  
Groves Dixon ◽  
Catherine L Peichel ◽  
...  
Keyword(s):  
Drosophila Melanogaster ◽  
Best Practices ◽  
Sex Chromosomes ◽  
Linkage Mapping ◽  
Poecilia Reticulata ◽  
Model Systems ◽  
History Of ◽  
Suppressed Recombination ◽  
Close Relatives

Abstract The sex chromosomes of the guppy, Poecilia reticulata, and its close relatives are of particular interest: they are much younger than the highly degenerate sex chromosomes of model systems such as humans and Drosophila melanogaster, and they carry many of the genes responsible for the males’ dramatic coloration. Over the last decade, several studies have analyzed these sex chromosomes using a variety of approaches including sequencing genomes and transcriptomes, cytology, and linkage mapping. Conflicting conclusions have emerged, in particular concerning the history of the sex chromosomes and the evolution of suppressed recombination between the X and Y. Here we address these controversies by reviewing the evidence and reanalyzing data. We find no evidence of a nonrecombining sex determining region (SDR) or evolutionary strata in P. reticulata. Further, we find that the data most strongly support the hypothesis that the SDRs of two close relatives of the guppy, P. wingei and Micropoecilia picta, evolved independently after their lineages diverged. We identify possible causes of conflicting results in previous studies and suggest best practices going forward.

scholarly journals Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers

2019 ◽  
Author(s):  
Iulia Darolti ◽  
Alison E. Wright ◽  
Benjamin A. Sandkam ◽  
Jake Morris ◽  
Natasha I. Bloch ◽  
...  
Keyword(s):  
Y Chromosome ◽  
Dosage Compensation ◽  
Sex Chromosomes ◽  
Poecilia Reticulata ◽  
Sex Chromosome ◽  
Sequencing Data ◽  
Chromosome Differentiation ◽  
Shared Ancestry ◽  
Sex Chromosome System ◽  
Suppressed Recombination

ABSTRACTOnce recombination is halted between the X and Y chromosome, sex chromosomes begin to differentiate and transition to heteromorphism. While there is a remarkable variation across clades in the degree of sex chromosome divergence, far less is known about variation in sex chromosome differentiation within clades. Here, we combined whole genome and transcriptome sequencing data to characterise the structure and conservation of sex chromosome systems across Poeciliidae, the livebearing clade that includes guppies. We found that the Poecilia reticulata XY system is much older than previously thought, being shared not only with its sister species, Poecilia wingei, but also with Poecilia picta, which diverged 30 mya. Despite the shared ancestry, we uncovered an extreme heterogeneity across these species in the proportion of the sex chromosome with suppressed recombination, and the degree of Y chromosome decay. The sex chromosomes in P. reticulata are largely homomorphic, with recombination persisting over a substantial fraction. However, the sex chromosomes in P. picta are completely non-recombining and strikingly heteromorphic. ln addition to being highly divergent, the sex chromosome system in P. picta includes a neo-sex chromosome, the result of a fusion between the ancestral sex chromosome and part of chromosome 7. Remarkably, the profound degradation of the ancestral Y chromosome in P. picta is counterbalanced by the evolution of complete dosage compensation in this species, the first such documented case in teleost fish. Our results offer important insight into the initial stages of sex chromosome evolution and dosage compensation.

scholarly journals Guppy Y Chromosome Integrity Maintained by Incomplete Recombination Suppression

2020 ◽  
Vol 12 (6) ◽  
pp. 965-977 ◽  
Author(s):  
Iulia Darolti ◽  
Alison E Wright ◽  
Judith E Mank
Keyword(s):  
Y Chromosome ◽  
X Chromosome ◽  
Sex Chromosomes ◽  
Poecilia Reticulata ◽  
Sex Chromosome ◽  
Rna Seq ◽  
Recombination Suppression ◽  
Sex Chromosome System ◽  
Chromosome Integrity ◽  
Heterogametic Sex

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.

scholarly journals Evolution of the canonical sex chromosomes of the guppy and its relatives

2020 ◽  
Author(s):  
M. Kirkpatrick ◽  
G. Dixon ◽  
J.M. Sardell ◽  
M. Schartl ◽  
C. L. Peichel
Keyword(s):  
Drosophila Melanogaster ◽  
Best Practices ◽  
Dosage Compensation ◽  
Sex Chromosomes ◽  
Linkage Mapping ◽  
Poecilia Reticulata ◽  
Model Systems ◽  
History Of ◽  
Suppressed Recombination ◽  
Close Relatives

AbstractThe sex chromosomes of the guppy, Poecilia reticulata, and its close relatives are of particular interest: they are much younger than the highly degenerate sex chromosomes of model systems such as mammals and Drosophila melanogaster, and they carry many of the genes responsible for the males’ dramatic coloration. Over the last decade, several studies have analyzed these sex chromosomes using a variety of approaches including sequencing genomes and transcriptomes, cytology, and linkage mapping. Conflicting conclusions have emerged, in particular concerning the history of the sex chromosomes and the evolution of suppressed recombination between the X and Y. Here we address these controversies by reviewing the evidence and reanalyzing data. We find no support for a nonrecombining sex determining region (SDR) or evolutionary strata in P. reticulata. We confirm that its congener P. picta has evolved dosage compensation across all of its X chromosome. Last, we do not find evidence that the nonrecombining SDRs of P. picta and P. wingei descend from a common ancestral SDR, and suggest instead that suppressed recombination between the X and Y evolved independently after the two species diverged. We identify possible causes of conflicting results in previous studies and suggest best practices going forward.

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

2020 ◽  
Author(s):  
Pedro Almeida ◽  
Benjamin A Sandkam ◽  
Jake Morris ◽  
Iulia Darolti ◽  
Felix Breden ◽  
...  
Keyword(s):  
Y Chromosome ◽  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Haplotype Diversity ◽  
Low Frequency ◽  
Color Variation ◽  
Recombination Suppression ◽  
Specific Sequence ◽  
Y Chromosome Evolution ◽  
Male Specific

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.

scholarly journals Contrasting tempos of sex chromosome degeneration in sticklebacks

2020 ◽  
Author(s):  
Jason M. Sardell ◽  
Matthew P. Josephson ◽  
Anne C. Dalziel ◽  
Catherine L. Peichel ◽  
Mark Kirkpatrick
Keyword(s):  
Sex Chromosomes ◽  
Gasterosteus Aculeatus ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Japan Sea ◽  
Chromosome 12 ◽  
Interspecific Crosses ◽  
Sex Chromosome Evolution ◽  
Recombination Suppression ◽  
Shared Ancestry

AbstractThe steps of sex chromosome evolution are often thought to follow a predictable pattern and tempo, but few studies have examined how the outcomes of this process differ between closely related species with homologous sex chromosomes. The sex chromosomes of the threespine stickleback (Gasterosteus aculeatus) and Japan Sea stickleback (G. nipponicus) have been well characterized. Little is known, however, about the sex chromosomes in their distantly related congener, the blackspotted stickleback (G. wheatlandi). We used pedigrees of interspecific crosses to obtain the first phased X and Y genomic sequences from blackspotted sticklebacks. Using novel statistical methods, we demonstrate that the oldest stratum of the Gasterosteus sex chromosomes evolved on Chromosome 19 in the ancestor of all three species. Despite this shared ancestry, the sex chromosomes of the blackspotted stickleback have experienced much more extensive recombination suppression, XY differentiation, and Y degeneration than those of the other two species. The ancestral blackspotted stickleback Y chromosome fused with Chromosome 12 less than 1.4 million years ago, which may have been favored by the very small size of the recombining region on the ancestral sex chromosome. Recombination is also suppressed between the X and Y over the bulk of Chromosome 12, although it has experienced little degeneration. These results demonstrate that sex chromosome evolution does not always follow a predictable tempo.

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

2020 ◽  
Author(s):  
Pedro Almeida ◽  
Benjamin A. Sandkam ◽  
Jake Morris ◽  
Iulia Darolti ◽  
Felix Breden ◽  
...  
Keyword(s):  
Y Chromosome ◽  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Haplotype Diversity ◽  
Low Frequency ◽  
Recombination Suppression ◽  
Specific Sequence ◽  
Y Chromosome Evolution ◽  
Male Specific ◽  
Genome Assemblies

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.

scholarly journals Evolution of recombination rates between sex chromosomes

2017 ◽  
Vol 372 (1736) ◽  
pp. 20160456 ◽  
Author(s):  
Deborah Charlesworth
Keyword(s):  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Molecular Genetic ◽  
Rate Variation ◽  
Recombination Rates ◽  
Recombination Suppression ◽  
Proximate Mechanisms ◽  
Chromosomal Heteromorphism ◽  
Suppressed Recombination ◽  
Recombination Rate Variation

In species with genetic sex-determination, the chromosomes carrying the sex-determining genes have often evolved non-recombining regions and subsequently evolved the full set of characteristics denoted by the term ‘sex chromosomes’. These include size differences, creating chromosomal heteromorphism, and loss of gene functions from one member of the chromosome pair. Such characteristics and changes have been widely reviewed, and underlie molecular genetic approaches that can detect sex chromosome regions. This review deals mainly with the evolution of new non-recombining regions, focusing on how certain evolutionary situations select for suppressed recombination (rather than the proximate mechanisms causing suppressed recombination between sex chromosomes). Particularly important is the likely involvement of sexually antagonistic polymorphisms in genome regions closely linked to sex-determining loci. These may be responsible for the evolutionary strata of sex chromosomes that have repeatedly formed by recombination suppression evolving across large genome regions. More studies of recently evolved non-recombining sex-determining regions should help to test this hypothesis empirically, and may provide evidence about whether other situations can sometimes lead to sex-linked regions evolving. Similarities with other non-recombining genome regions are discussed briefly, to illustrate common features of the different cases, though no general properties apply to all of them. This article is part of the themed issue ‘Evolutionary causes and consequences of recombination rate variation in sexual organisms’.

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