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A reciprocal translocation radically reshapes sex-linked inheritance in the common frog.

ABSTRACT: X and Y chromosomes can diverge when rearrangements block recombination between them. Here we present the first genomic view of a reciprocal translocation that causes two physically unconnected pairs of chromosomes to be coinherited as sex chromosomes. In a population of the common frog (Rana temporaria), both pairs of X and Y chromosomes show extensive sequence differentiation, but not degeneration of the Y chromosomes. A new method based on gene trees shows both chromosomes are sex-linked. Furthermore, the gene trees from the two Y chromosomes have identical topologies, showing they have been coinherited since the reciprocal translocation occurred. Reciprocal translocations can thus reshape sex linkage on a much greater scale compared with inversions, the type of rearrangement that is much better known in sex chromosome evolution, and they can greatly amplify the power of sexually antagonistic selection to drive genomic rearrangement. Two more populations show evidence of other rearrangements, suggesting that this species has unprecedented structural polymorphism in its sex chromosomes.

SUBMITTER: Toups MA

PROVIDER: S-EPMC7558804 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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A reciprocal translocation radically reshapes sex-linked inheritance in the common frog.

Toups Melissa A MA Rodrigues Nicolas N Perrin Nicolas N Kirkpatrick Mark M

Molecular ecology 20190429 8

X and Y chromosomes can diverge when rearrangements block recombination between them. Here we present the first genomic view of a reciprocal translocation that causes two physically unconnected pairs of chromosomes to be coinherited as sex chromosomes. In a population of the common frog (Rana temporaria), both pairs of X and Y chromosomes show extensive sequence differentiation, but not degeneration of the Y chromosomes. A new method based on gene trees shows both chromosomes are sex-linked. Fur ...[more]

PMID: 30576024

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Project description:Chromosome rearrangements (CRs) are perceived to be related to sex chromosome evolution, but it is a matter of controversy whether CRs are the initial causative mechanism of suppressed recombination for sex differentiation. The early stages of sex chromosome evolution in amphibians may represent intermediate states of differentiation, and if so, they potentially shed light on the ultimate cause of suppressed recombination and the role of CRs in sex chromosome differentiation. In this paper, we showed that sex determination differs among 16 populations of spiny frog (Quasipaa boulengeri), in which individuals have normal and rearranged chromosomes caused by reciprocal translocation. In eastern areas, without translocation, genetic differentiation between sexes was relatively low, suggesting unrestricted recombination. In comparison, in western populations that have both normal and translocated chromosomes, a male-heterogametic system and lack of X-Y recombination were identified by male-specific alleles and heterozygote excess. However, such genetic differentiation between sexes in western populations was not directly related to karyotypes, as it was found in individuals with both normal and translocated karyotypes. In the western Sichuan Basin, male-specific and translocation-specific allelic frequency distributions suggested that recombination of sex-differentiation ceased in all populations, but recombination suppression caused by translocation did not exist in some populations. Combined with phylogenetic inference, this indicated that the establishment of sex-linkage had taken place independently of reciprocal translocation, and translocation was not the ultimate cause of sex chromosome differentiation. Furthermore, comparison of the genetic diversity of alleles on Y chromosomes, X chromosomes, and autosomes in western populations showed a reduction of effective population size on sex chromosomes, which may be caused by reciprocal translocation. It indicates that, although it is not the ultimate cause of recombination suppression, reciprocal translocation may enhance sex chromosome differentiation.

Project description:The extent to which sex reversal is associated with transitions in sex determining systems (XX-XY, ZZ-ZW, etc.) or abnormal sexual differentiation is predominantly unexplored in amphibians. This is in large part because most amphibian taxa have homomorphic sex chromosomes, which has traditionally made it challenging to identify discordance between phenotypic and genetic sex in amphibians, despite all amphibians having a genetic component to sex determination. Recent advances in molecular techniques such as genome complexity reduction and high throughput sequencing present a valuable avenue for furthering our understanding of sex determination in amphibians and other taxa with homomorphic sex chromosomes like many fish and reptiles.We use DArTseq as a novel approach to identify sex-linked markers in the North American green frog (Rana clamitans melanota) using lab-reared tadpoles as well as wild-caught adults from seven ponds either in undeveloped, forested habitats or suburban ponds known to be subject to contamination by anthropogenic chemicals. The DArTseq methodology identified 13 sex-linked SNP loci and eight presence-absence loci associated with males, indicating an XX-XY system. Both alleles from a single locus show partial high sequence homology to Dmrt1, a gene linked to sex determination and differentiation throughout Metazoa. Two other loci have sequence similarities to regions of the chimpanzee and human X-chromosome as well as the chicken Z-chromosome. Several loci also show geographic variation in sex-linkage, possibly indicating sex chromosome recombination. While all loci are statistically sex-linked, they show varying degrees of female heterozygosity and male homozygosity, providing further evidence that some markers are on regions of the sex chromosomes undergoing higher rates of recombination and therefore further apart from the putative sex determining locus.The ease of the DArTseq platform provides a useful avenue for future research on sex reversal and sex chromosome evolution in vertebrates, particularly for non-model species with homomorphic or cryptic or nascent sex chromosomes.

Dataset Information

A reciprocal translocation radically reshapes sex-linked inheritance in the common frog.

Publications

A reciprocal translocation radically reshapes sex-linked inheritance in the common frog.

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