Sex determining gene transposition as an evolutionary platform for chromosome turnover

Ayllón, Fernando; Solberg, Monica Favnebøe; Besnier, François; Fjelldal, Per Gunnar; Hansen, Tom; Wargelius, Anna; Edvardsen, Rolf B.; Glover, Kevin A.

doi:10.1101/2020.03.14.991026

Cited by 4 publications

(5 citation statements)

References 52 publications

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“…It is also congruous with a previous study finding a high percentage of sdY-negative sockeye salmon males (~30%) in an upper Columbia River hatchery [ 27 ], and another study with similar findings in samples collected from Asian populations [ 147 ]. Atlantic salmon females have been identified with sdY, but likely have autosomal pseudocopies rather than a bonafide function sex-determining copy (bioRχiv [ 148 ]) [ 33 ]. This has been noted in other salmonid species as well [ 147 ].…”

Section: Discussionmentioning

confidence: 99%

The sockeye salmon genome, transcriptome, and analyses identifying population defining regions of the genome

et al. 2020

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Sockeye salmon ( Oncorhynchus nerka ) is a commercially and culturally important species to the people that live along the northern Pacific Ocean coast. There are two main sockeye salmon ecotypes—the ocean-going (anadromous) ecotype and the fresh-water ecotype known as kokanee. The goal of this study was to better understand the population structure of sockeye salmon and identify possible genomic differences among populations and between the two ecotypes. In pursuit of this goal, we generated the first reference sockeye salmon genome assembly and an RNA-seq transcriptome data set to better annotate features of the assembly. Resequenced whole-genomes of 140 sockeye salmon and kokanee were analyzed to understand population structure and identify genomic differences between ecotypes. Three distinct geographic and genetic groups were identified from analyses of the resequencing data. Nucleotide variants in an immunoglobulin heavy chain variable gene cluster on chromosome 26 were found to differentiate the northwestern group from the southern and upper Columbia River groups. Several candidate genes were found to be associated with the kokanee ecotype. Many of these genes were related to ammonia tolerance or vision. Finally, the sex chromosomes of this species were better characterized, and an alternative sex-determination mechanism was identified in a subset of upper Columbia River kokanee.

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Section: Discussionmentioning

confidence: 99%

The sockeye salmon genome, transcriptome, and analyses identifying population defining regions of the genome

et al. 2020

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“…Although there are many exceptions, heterogametic sex chromosomes are thought to form from ancestral autosomes through a process involving acquisition of a master sex determining locus, suppression of recombination, divergence, degeneration, and eventual loss of the reduced sex chromosome, with turnover potentially occurring at any stage of this cycle (Furman et al, 2020). Autosomes can become sex chromosomes via the emergence of novel factors controlling sexual determination (e.gHerpin et al, 2010;Zhang, 2004) or transposition of an existing sex-determining factor (e.g Ayllon et al, 2020;Traut & Willhoeft, 1990). Furthermore, theory predicts that transitions between sexual determination systems can occur without change in the primary factor or sex chromosomes when the pathway underlying sexual determination is sensitive to environmental conditions (Quinn et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Chromosome level reference of Atlantic halibut Hippoglossushippoglossus provides insight into the evolution of sexual determination systems

Einfeldt

Kess

Messmer

et al. 2021

Molecular Ecology Resources

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Changes in the genetic mechanisms that control sexual determination have occurred independently across the tree of life, and with exceptional frequency in teleost fishes.To investigate the genomic changes underlying the evolution of sexual determination, we sequenced a chromosome-level genome, multitissue transcriptomes, and reduced representation population data for the Atlantic halibut (Hippoglossus hippoglossus), which has an XY/XX sex determination mechanism and has recently diverged (0.9-3.8 Ma) from the Pacific halibut (Hippoglossus stenolepis), which has a ZZ/ZW system.We used frequency and coverage-based population approaches to identify a putative sex-determining factor, GSDF. We characterized regions with elevated heterozygosity and linkage disequilibrium indicating suppression of recombination across a nascent sex chromosome. We detected testis-specific expression of GSDF, the sequence of which is highly conserved across flatfishes. Based on evidence from genome-wide association, coverage, linkage disequilibrium, testis and brain transcriptomes, and sequence conservation with other flatfishes, we propose a mechanism for the recent evolution of an XY sex-determination mechanism in Atlantic halibut. Changes to the ancestral sex-determining gene DMRT1 in regulating the downstream gene GSDF probably coincided with GSDF, or a proximal regulatory element of it, becoming the primary sex-determining factor. Our results suggest changes to a small number of elements can have drastic repercussions for the genomic substrate available to sex-specific evolutionary forces, providing insight into how certain elements repeatedly evolve to control sex across taxa. Our chromosome-level assembly, multitissue transcriptomes, and population genomic data provide a valuable resource and understanding of the evolution of sexual systems in fishes. K E Y W O R D Sevolution of sex, fish, genome-wide association analyses, pleuronectiformes, sex chromosome turnover | 1687 EINFELDT ET aL.

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“…Emily K. Glover is gratefully acknowledged for drawing the salmon used in Figures 3 , 4 . This manuscript has been released as a pre-print at BioRxiv ( Ayllon et al, 2020 ).…”

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Autosomal sdY Pseudogenes Explain Discordances Between Phenotypic Sex and DNA Marker for Sex Identification in Atlantic Salmon

et al. 2020

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Despite the key role that sex-determination plays in evolutionary processes, it is still poorly understood in many species. In salmonids, which are among the best studied fishes, the master sex-determining gene sexually dimorphic on the Y-chromosome ( sdY ) has been identified. However, sdY displays unexplained discordance to the phenotypic sex, with a variable frequency of phenotypic females being reported as genetic males. Multiple sex determining loci in Atlantic salmon have also been reported, possibly as a result of recent transposition events in this species. We hypothesized the existence of an autosomal copy of sdY , causing apparent discordance between phenotypic and genetic sex, that is transmitted in accordance with autosomal inheritance. To test this, we developed a qPCR methodology to detect the total number of sdY copies present in the genome. Based on the observed phenotype/genotype frequencies and linkage analysis among 2,025 offspring from 64 pedigree-controlled families of accurately phenotyped Atlantic salmon, we identified both males and females carrying one or two autosomal copies of sdY in addition to the Y-specific copy present in males. Patterns across families were highly consistent with autosomal inheritance. These autosomal sdY copies appear to have lost the ability to function as a sex determining gene and were only occasionally assigned to the actual sex chromosome in any of the affected families.

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Sex determining gene transposition as an evolutionary platform for chromosome turnover

Cited by 4 publications

References 52 publications

The sockeye salmon genome, transcriptome, and analyses identifying population defining regions of the genome

The sockeye salmon genome, transcriptome, and analyses identifying population defining regions of the genome

Chromosome level reference of Atlantic halibut Hippoglossushippoglossus provides insight into the evolution of sexual determination systems

Autosomal sdY Pseudogenes Explain Discordances Between Phenotypic Sex and DNA Marker for Sex Identification in Atlantic Salmon

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