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Research article - Peer-reviewed, 2020

Reconstruction of the birth of a male sex chromosome present in Atlantic herring

Rafati, Nima; Chen, Junfeng; Herpin, Amaury; Pettersson, Mats E.; Han, Fan; Feng, Chungang; Wallerman, Ola; Rubin, Carl-Johan; Peron, Sandrine; Cocco, Arianna; Larsson, Marten; Troetschel, Christian; Poetsch, Ansgar; Korsching, Kai; Boenigk, Wolfgang; Koerschen, Heinz G.; Berg, Florian; Folkvord, Arild; Kaupp, U. Benjamin; Schartl, Manfred;
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Abstract

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 similar to 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.

Keywords

sex determination; BMPR1; CatSper; gene duplication; molecular evolution

Published in

Proceedings of the National Academy of Sciences of the United States of America
2020, volume: 117, number: 39, pages: 24359-24368
Publisher: NATL ACAD SCIENCES

Authors' information

Rafati, Nima
Uppsala University
Chen, Junfeng
Uppsala University
Herpin, Amaury
Hunan Normal University
Pettersson, Mats E.
Uppsala University
Han, Fan
Uppsala University
Feng, Chungang
Uppsala University
Wallerman, Ola
Uppsala University
Rubin, Carl-Johan
Uppsala University
Peron, Sandrine
INRAE
Cocco, Arianna
Uppsala University
Larsson, Marten
Uppsala University
Troetschel, Christian
Ruhr University Bochum
Poetsch, Ansgar
Ruhr University Bochum
Korsching, Kai
Center of Advanced European Study and Research (CAESAR)
Bönigk, Wolfgang
Center of Advanced European Study and Research (CAESAR)
Körschen, Heinz G.
Center of Advanced European Study and Research (CAESAR)
Berg, Florian
University of Bergen
Folkvord, Arild
University of Bergen
Kaupp, U. Benjamin
University of Bonn
Schartl, Manfred
University of Wurzburg
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UKÄ Subject classification

Evolutionary Biology

Publication Identifiers

DOI: https://doi.org/10.1073/pnas.2009925117

URI (permanent link to this page)

https://res.slu.se/id/publ/108385