Heterochiasmy and the establishment of gsdf as a novel sex determining gene in Atlantic halibut

Rolf Brudvik Edvardsen; Ola Wallerman; Tomasz Furmanek; Lene Kleppe; Patric Jern; Andreas Wallberg; Erik Kjærner-Semb; Stig Mæhle; Sara Karolina Olausson; Elisabeth Sundström; Torstein Harboe; Ragnfrid Mangor-Jensen; Margareth Møgster; Prescilla Perrichon; Birgitta Norberg; Carl-Johan Rubin

doi:10.1371/journal.pgen.1010011

Heterochiasmy and the establishment of gsdf as a novel sex determining gene in Atlantic halibut

PLoS Genet. 2022 Feb 8;18(2):e1010011. doi: 10.1371/journal.pgen.1010011. eCollection 2022 Feb.

Authors

Rolf Brudvik Edvardsen¹, Ola Wallerman², Tomasz Furmanek¹, Lene Kleppe¹, Patric Jern², Andreas Wallberg², Erik Kjærner-Semb¹, Stig Mæhle¹, Sara Karolina Olausson³, Elisabeth Sundström², Torstein Harboe³, Ragnfrid Mangor-Jensen³, Margareth Møgster³, Prescilla Perrichon³, Birgitta Norberg³, Carl-Johan Rubin^{1

2}

Affiliations

¹ Institute of Marine Research, Bergen, Norway.
² Uppsala University, Uppsala, Sweden.
³ Institute of Marine Research, Storebø, Norway.

Abstract

Atlantic Halibut (Hippoglossus hippoglossus) has a X/Y genetic sex determination system, but the sex determining factor is not known. We produced a high-quality genome assembly from a male and identified parts of chromosome 13 as the Y chromosome due to sequence divergence between sexes and segregation of sex genotypes in pedigrees. Linkage analysis revealed that all chromosomes exhibit heterochiasmy, i.e. male-only and female-only meiotic recombination regions (MRR/FRR). We show that FRR/MRR intervals differ in nucleotide diversity and repeat class content and that this is true also for other Pleuronectidae species. We further show that remnants of a Gypsy-like transposable element insertion on chr13 promotes early male specific expression of gonadal somatic cell derived factor (gsdf). Less than 4.5 MYA, this male-determining element evolved on an autosomal FRR segment featuring pre-existing male meiotic recombination barriers, thereby creating a Y chromosome. Our findings indicate that heterochiasmy may facilitate the evolution of genetic sex determination systems relying on linkage of sexually antagonistic loci to a sex-determining factor.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
DNA Transposable Elements
Embryo, Nonmammalian
Female
Fish Proteins / genetics*
Flounder / embryology
Flounder / genetics*
Gene Expression
Genome
Male
Meiosis
Promoter Regions, Genetic
Recombination, Genetic*
Repetitive Sequences, Nucleic Acid
Sex Chromosomes
Sex Determination Processes*
Y Chromosome

Substances

DNA Transposable Elements
Fish Proteins

Grants and funding

We are grateful for financial support from Sterling White Halibut (https://sterlingwhitehalibut.com/en) to B.N. for the sex determining factor part of this work. This study was co-funded by the Norwegian Ministry of Trade, Industry and Fisheries through its funding of the Institute of Marine Research (https://www.hi.no/en) to RBE. This research was supported by grants from the Swedish Research Council Formas (https://formas.se/en/start-page.html) (2012-00740 to C.J.R.; 2018-01008 to P.J.; 2017-00413 to A.W) and Vetenskapsrådet (https://www.vr.se/english.html) 2018-03017 to P.J.; 2018-04444 to A.W.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.