TY - JOUR
T1 - Aberrant X chromosome dosage compensation causes hybrid male inviability in Caenorhabditis
AU - Li, Yongbin
AU - Gao, Yimeng
AU - Ma, Jiaonv
AU - Gao, Yifan
AU - Tang, Jiemei
AU - Yang, Rui
AU - Wang, Jiajia
AU - Zhou, Wangyan
AU - Zhang, Hantang
AU - Shao, Wenhua
AU - Liu, Zhijin
AU - Zhao, Zhongying
AU - Liu, Xiao
N1 - Funding: National Natural Science Foundation of China Grant 31861163005 (X.L.) National Natural Science Foundation of China Grant 32400501 (Y.L.) National Natural Science Foundation of China Grant 32470653 (X.L.) National Natural Science Foundation of China Grant 31871472 (X.L.) National Natural Science Foundation of China Grant 32070639 (X.L.) R&D Program of Beijing Municipal Education Commission Grant KM202310028008 (Y.L.)
Publisher Copyright:
Copyright © 2025 the Author(s).
PY - 2025/10/28
Y1 - 2025/10/28
N2 - Zygotic reproductive isolation frequently initiates with hybrid incompatibility in the heterogametic sex, such as males in XX/XY systems. The genetic basis of hybrid male incompatibility has long remained elusive. Here, we show that crosses of Caenorhabditis nigoni males with C. briggsae females result in insufficient expression of Cbr-xol-1, an X-linked master switch responsible for intimately linked sex determination and dosage compensation pathways, consequently triggering aberrant X-chromosome repression in males, and ultimately leading to embryonic inviability. In contrast, male embryos from the reciprocal cross maintain normal expression level of C. nigoni xol-1 genes, consistent with their viability. We further demonstrate that the cis-regulatory regions of Cbr-xol-1 and Cni-xol-1 have functionally diverged. Finally, X transcription is also aberrantly repressed in lethal hybrid male embryos from crosses between gonochoristic species C. latens and C. remanei. Our results suggest an evolutionary scenario in which incompatibility of the dosage compensation system leads to reproductive isolation.
AB - Zygotic reproductive isolation frequently initiates with hybrid incompatibility in the heterogametic sex, such as males in XX/XY systems. The genetic basis of hybrid male incompatibility has long remained elusive. Here, we show that crosses of Caenorhabditis nigoni males with C. briggsae females result in insufficient expression of Cbr-xol-1, an X-linked master switch responsible for intimately linked sex determination and dosage compensation pathways, consequently triggering aberrant X-chromosome repression in males, and ultimately leading to embryonic inviability. In contrast, male embryos from the reciprocal cross maintain normal expression level of C. nigoni xol-1 genes, consistent with their viability. We further demonstrate that the cis-regulatory regions of Cbr-xol-1 and Cni-xol-1 have functionally diverged. Finally, X transcription is also aberrantly repressed in lethal hybrid male embryos from crosses between gonochoristic species C. latens and C. remanei. Our results suggest an evolutionary scenario in which incompatibility of the dosage compensation system leads to reproductive isolation.
KW - Caenorhabditis
KW - dosage compensation
KW - Haledane’s rule
KW - hybrid male incompatibility
KW - xol-1
UR - http://www.scopus.com/inward/record.url?scp=105019822606&partnerID=8YFLogxK
UR - https://www.pnas.org/doi/10.1073/pnas.2507166122
U2 - 10.1073/pnas.2507166122
DO - 10.1073/pnas.2507166122
M3 - Journal article
C2 - 41129226
AN - SCOPUS:105019822606
SN - 0027-8424
VL - 122
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 43
M1 - e2507166122
ER -
