A single-nucleus RNA atlas of the hedgehog testis reveals the cellular basis of seasonal reproduction
- 1Guangdong Provincial Key Laboratory of Marine Biotechnology, Shantou University, Shantou 515063, China
- 2Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou 511458, China
Abstract
Seasonal reproduction in mammals entails profound functional remodeling of the testis, yet the underlying cellular and molecular mechanisms remain incompletely understood. Here, we employed single-nucleus RNA sequencing (snRNA-seq) to profile testes from reproductive and non-reproductive stages of the four-toed hedgehog (Atelerix albiventris), a representative seasonal breeder exhibiting reversible transitions in reproductive function. By analyzing 16,901 nuclei, we identified 12 major cell types that were consistently preserved across stages, with comparable cell abundances, indicating that seasonal reproductive transitions might rely primarily on functional modulation rather than loss or gain of cellular lineages. This stability was further supported by highly conserved transcriptomic identities across stages. Despite this overall conservation, localized cell subtype compositional and transcriptional changes were primarily detected in spermatogonia, late spermatids, and immune cells. Trajectory analysis revealed that inactivation of spermatogenesis in the non-reproductive stage is driven by a differentiation checkpoint at the transition from committed to pre-meiotic spermatogonia. This gating is associated with upregulated calcium signaling and enhanced post-transcriptional regulation during the reproductive stage, whereas its disruption leads to the accumulation of committed spermatogonia in the non-reproductive stage. Concurrently, mature spermatozoa are still retained during the non-reproductive stage and exhibit survival-oriented programs involving enhanced mitochondrial and proteostasis regulation. In parallel, the testicular immune microenvironment undergoes pronounced seasonal reprogramming, characterized by the polarization of lymphoid cells and macrophages toward immune tolerance and homeostatic maintenance in the non-reproductive stage. Together, these findings demonstrate that transitions in reproductive function in the four-toed hedgehog testis are governed by coordinated regulation of spermatogonia differentiation gating, spermatozoa metabolic reprogramming, and immune microenvironmental remodeling, providing a comprehensive cellular framework for understanding seasonal reproduction and adaptations in mammals.
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BibTeX
@article{zhu2026singlenucleus,
title = {{A single-nucleus RNA atlas of the hedgehog testis reveals the cellular basis of seasonal reproduction}},
author = {Chu-wen Zhu and Wen-hua Liu and Guang Yang and Si-min Chai},
journal = {Journal of Zoological Systematics and Evolutionary Research},
year = {2026},
month = jul,
doi = {10.48130/jzser-0026-0007},
url = {https://doi.org/10.48130/jzser-0026-0007},
note = {CC BY},
}
RIS
TY - JOUR
TI - A single-nucleus RNA atlas of the hedgehog testis reveals the cellular basis of seasonal reproduction
AU - Chu-wen Zhu
AU - Wen-hua Liu
AU - Guang Yang
AU - Si-min Chai
PY - 2026
DA - 2026/07/01
JO - Journal of Zoological Systematics and Evolutionary Research
DO - 10.48130/jzser-0026-0007
UR - https://doi.org/10.48130/jzser-0026-0007
AB - Seasonal reproduction in mammals entails profound functional remodeling of the testis, yet the underlying cellular and molecular mechanisms remain incompletely understood. Here, we employed single-nucleus RNA sequencing (snRNA-seq) to profile testes from reproductive and non-reproductive stages of the four-toed hedgehog (Atelerix albiventris), a representative seasonal breeder exhibiting reversible transitions in reproductive function. By analyzing 16,901 nuclei, we identified 12 major cell types that were consistently preserved across stages, with comparable cell abundances, indicating that seasonal reproductive transitions might rely primarily on functional modulation rather than loss or gain of cellular lineages. This stability was further supported by highly conserved transcriptomic identities across stages. Despite this overall conservation, localized cell subtype compositional and transcriptional changes were primarily detected in spermatogonia, late spermatids, and immune cells. Trajectory analysis revealed that inactivation of spermatogenesis in the non-reproductive stage is driven by a differentiation checkpoint at the transition from committed to pre-meiotic spermatogonia. This gating is associated with upregulated calcium signaling and enhanced post-transcriptional regulation during the reproductive stage, whereas its disruption leads to the accumulation of committed spermatogonia in the non-reproductive stage. Concurrently, mature spermatozoa are still retained during the non-reproductive stage and exhibit survival-oriented programs involving enhanced mitochondrial and proteostasis regulation. In parallel, the testicular immune microenvironment undergoes pronounced seasonal reprogramming, characterized by the polarization of lymphoid cells and macrophages toward immune tolerance and homeostatic maintenance in the non-reproductive stage. Together, these findings demonstrate that transitions in reproductive function in the four-toed hedgehog testis are governed by coordinated regulation of spermatogonia differentiation gating, spermatozoa metabolic reprogramming, and immune microenvironmental remodeling, providing a comprehensive cellular framework for understanding seasonal reproduction and adaptations in mammals.
SN - 1439-0469
SN - 0947-5745
ER -