TY - JOUR
T1 - Independent evolution of sex chromosomes and male pregnancy-related genes in two seahorse species
AU - Long, Xin
AU - Charlesworth, Deborah
AU - Qi, Jianfei
AU - Wu, Ruiqiong
AU - Chen, Meiling
AU - Wang, Zongji
AU - Xu, Luohao
AU - Fu, Honggao
AU - Zhang, Xueping
AU - Chen, Xinxin
AU - He, Libin
AU - Zheng, Leyun
AU - Huang, Zhen
AU - Zhou, Qi
A2 - Wilson, Melissa
N1 - Funding Information:
Animal icons are from https://thenounproject.com (including “Testis” icon by Becris, “Ovary” icon by Dairy Free Design, “Kidney” icon by Alexander Blagochevsky, “Muscle” icon by Tezar Tantular, “Brain” icon by Pixel Bazaar, and “Garfish” icon by Phạm Thanh Lộc). This work is supported by the National Natural Science Foundation of China (32170415 and 32061130208), Natural Science Foundation of Zhejiang Province (LD19C190001), European Research Council Starting Grant (grant agreement 677696) to Q.Z., and the 13th Five-Year Plan for the Marine Innovation and Economic Development Demonstration Projects (FZHJ11) to Z.H.
Publisher Copyright:
© 2022 The Author(s). Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.
PY - 2023/1/1
Y1 - 2023/1/1
N2 - Unlike birds and mammals, many teleosts have homomorphic sex chromosomes, and changes in the chromosome carrying the sex-determining locus, termed "turnovers", are common. Recent turnovers allow studies of several interesting questions. One question is whether the new sex-determining regions evolve to become completely non-recombining, and if so, how and why. Another is whether (as predicted) evolutionary changes that benefit one sex accumulate in the newly sex-linked region. To study these questions, we analyzed the genome sequences of two seahorse species of the Syngnathidae, a fish group in which many species evolved a unique structure, the male brood pouch. We find that both seahorse species have XY sex chromosome systems, but their sex chromosome pairs are not homologs, implying that at least one turnover event has occurred. The Y-linked regions occupy 63.9% and 95.1% of the entire sex chromosome of the two species and do not exhibit extensive sequence divergence with their X-linked homologs. We find evidence for occasional recombination between the extant sex chromosomes that may account for their homomorphism. We argue that these Y-linked regions did not evolve by recombination suppression after the turnover, but by the ancestral nature of the low crossover rates in these chromosome regions. With such an ancestral crossover landscape, a turnover can instantly create an extensive Y-linked region. Finally, we test for adaptive evolution of male pouch-related genes after they became Y-linked in the seahorse.
AB - Unlike birds and mammals, many teleosts have homomorphic sex chromosomes, and changes in the chromosome carrying the sex-determining locus, termed "turnovers", are common. Recent turnovers allow studies of several interesting questions. One question is whether the new sex-determining regions evolve to become completely non-recombining, and if so, how and why. Another is whether (as predicted) evolutionary changes that benefit one sex accumulate in the newly sex-linked region. To study these questions, we analyzed the genome sequences of two seahorse species of the Syngnathidae, a fish group in which many species evolved a unique structure, the male brood pouch. We find that both seahorse species have XY sex chromosome systems, but their sex chromosome pairs are not homologs, implying that at least one turnover event has occurred. The Y-linked regions occupy 63.9% and 95.1% of the entire sex chromosome of the two species and do not exhibit extensive sequence divergence with their X-linked homologs. We find evidence for occasional recombination between the extant sex chromosomes that may account for their homomorphism. We argue that these Y-linked regions did not evolve by recombination suppression after the turnover, but by the ancestral nature of the low crossover rates in these chromosome regions. With such an ancestral crossover landscape, a turnover can instantly create an extensive Y-linked region. Finally, we test for adaptive evolution of male pouch-related genes after they became Y-linked in the seahorse.
KW - seahorse
KW - sex chromosome
KW - genome evolution
U2 - 10.1093/molbev/msac279
DO - 10.1093/molbev/msac279
M3 - Article
C2 - 36578180
SN - 0737-4038
VL - 40
JO - Molecular Biology and Evolution
JF - Molecular Biology and Evolution
IS - 1
M1 - msac279
ER -