{"title":"Coordinated Transcriptomic and Epigenetic Approach Reveals Molecular Features Underlying Natural Mating Ability in Captive Male Giant Pandas","authors":"Zheng Yan, Yinghu Lei, Pengpeng Zhao, Danhui Zhang, Jiena Shen, Guiquan Zhang, Rongping Wei, Mingyue Zhang, Dingzhen Liu","doi":"10.1002/ece3.72283","DOIUrl":null,"url":null,"abstract":"<p>Natural mating ability is a critical behavioral trait for the reproductive success of captive endangered mammals, and its loss often reflects declining adaptability and potential physiological dysfunctions. However, the underlying molecular regulatory mechanisms remain poorly understood. In this study, we integrated blood transcriptome and whole-genome DNA methylation (whole-genome bisulfite sequencing) data to systematically explore the molecular basis of natural mating ability differences in captive male giant pandas (<i>Ailuropoda melanoleuca</i>). A total of 21 male individuals, which were classified into either capable (with successful natural mating experience) or incapable (with repeated mating failure despite physical health) groups, were sampled from three breeding centers. RNA-seq analysis identified key differentially expressed genes (DEGs) such as <i>ZPBP2</i>, enriched in functional pathways related to GnRH signaling, MAPK cascades, immune modulation, and olfactory perception. Whole-genome bisulfite sequencing (WGBS) analysis revealed significant differences in CpG (CG) methylation density on the X chromosome, and identified promoter- and gene body-associated differentially methylated regions (DMRs) that were inversely correlated with gene expression. Integrative analysis demonstrated a strong association between gene expression and DNA methylation, with the associated genes enriched in reproduction-relevant pathways including axon guidance, cysteine and methionine metabolism, and apoptosis/autophagy. These findings suggest that DNA methylation may influence transcriptional activity involved in natural mating behavior. This multi-omics approach provides valuable insights into the epigenetic regulation of complex reproductive phenotypes in endangered species and offers a theoretical basis for future applications in molecular marker–based individual selection and optimization of captive breeding programs, thereby contributing to wildlife conservation efforts.</p>","PeriodicalId":11467,"journal":{"name":"Ecology and Evolution","volume":"15 10","pages":""},"PeriodicalIF":2.3000,"publicationDate":"2025-10-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12516017/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Ecology and Evolution","FirstCategoryId":"99","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1002/ece3.72283","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"ECOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Natural mating ability is a critical behavioral trait for the reproductive success of captive endangered mammals, and its loss often reflects declining adaptability and potential physiological dysfunctions. However, the underlying molecular regulatory mechanisms remain poorly understood. In this study, we integrated blood transcriptome and whole-genome DNA methylation (whole-genome bisulfite sequencing) data to systematically explore the molecular basis of natural mating ability differences in captive male giant pandas (Ailuropoda melanoleuca). A total of 21 male individuals, which were classified into either capable (with successful natural mating experience) or incapable (with repeated mating failure despite physical health) groups, were sampled from three breeding centers. RNA-seq analysis identified key differentially expressed genes (DEGs) such as ZPBP2, enriched in functional pathways related to GnRH signaling, MAPK cascades, immune modulation, and olfactory perception. Whole-genome bisulfite sequencing (WGBS) analysis revealed significant differences in CpG (CG) methylation density on the X chromosome, and identified promoter- and gene body-associated differentially methylated regions (DMRs) that were inversely correlated with gene expression. Integrative analysis demonstrated a strong association between gene expression and DNA methylation, with the associated genes enriched in reproduction-relevant pathways including axon guidance, cysteine and methionine metabolism, and apoptosis/autophagy. These findings suggest that DNA methylation may influence transcriptional activity involved in natural mating behavior. This multi-omics approach provides valuable insights into the epigenetic regulation of complex reproductive phenotypes in endangered species and offers a theoretical basis for future applications in molecular marker–based individual selection and optimization of captive breeding programs, thereby contributing to wildlife conservation efforts.
期刊介绍:
Ecology and Evolution is the peer reviewed journal for rapid dissemination of research in all areas of ecology, evolution and conservation science. The journal gives priority to quality research reports, theoretical or empirical, that develop our understanding of organisms and their diversity, interactions between them, and the natural environment.
Ecology and Evolution gives prompt and equal consideration to papers reporting theoretical, experimental, applied and descriptive work in terrestrial and aquatic environments. The journal will consider submissions across taxa in areas including but not limited to micro and macro ecological and evolutionary processes, characteristics of and interactions between individuals, populations, communities and the environment, physiological responses to environmental change, population genetics and phylogenetics, relatedness and kin selection, life histories, systematics and taxonomy, conservation genetics, extinction, speciation, adaption, behaviour, biodiversity, species abundance, macroecology, population and ecosystem dynamics, and conservation policy.