Transcriptomic analysis of paternal behaviors in prairie voles.
Transcriptomic analysis of paternal behaviors in prairie voles.
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DOI：
10.1186/s12864-022-08912-y
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发表时间：
2022-10-01
期刊：
影响因子：
4.4
通讯作者：
中科院分区：
文献类型：
--
作者：
父亲参与照料的重要性及其在子女认知和情感发展中的关键作用现已得到充分确认。然而，由于缺乏合适的动物模型，对潜在的神经生物学知之甚少。在社会性一夫一妻制和双亲草原田鼠（Microtus ochrogaster）中，60-80%的处女雄性表现出自发的父性行为（父性），其他则表现出小狗定向的攻击（攻击者）。在这里，我们利用这种表型二分法，并在三个重要的大脑区域使用RNA测序来表征与父系男性的父系行为相关的基因表达，并将其与有经验的父亲和母亲进行比较。虽然父亲的男性表现出相同的范围和程度的父亲的行为，有经验的父亲，我们观察到的结构特异性转录组的父母的行为表型之间的差异。利用差异表达、基因集表达以及共表达网络分析，我们发现父本雄性和攻击者之间的表型差异主要反映在外侧隔（LS）上，在较低程度上反映在外侧隔核（NAc）、转录组上。在内侧视前区（MPOA），基因表达谱主要反映了雌性和雄性之间的差异，而与其亲本行为表型无关。与LS和NAc中的父系男性或攻击者相关的那些基因集的功能富集分析揭示了与线粒体、RNA翻译、蛋白质降解过程以及基因表达的表观遗传调节相关的过程的参与。通过利用自然表型差异的父母的行为在处女雄性草原田鼠的父亲和母亲，我们确定了一个显着的结构和表型特异性模式的基因表达与自发的父系行为独立于父亲和配对。因此，与线粒体、RNA翻译和蛋白质降解过程相关的LS转录组被强调为与父性行为的自发显示相关的主要候选者。总之，我们的观察结果进一步表征了社会一夫一妻制草原田鼠中父母行为的行为和转录组学特征，并为进一步理解父亲行为的分子基础奠定了基础。在线版本包含补充材料，可通过10.1186/s12864-022-08912-y获得。
The importance of fathers’ engagement in care and its critical role in the offspring’s cognitive and emotional development is now well established. Yet, little is known on the underlying neurobiology due to the lack of appropriate animal models. In the socially monogamous and bi-parental prairie vole (Microtus ochrogaster), while 60–80% of virgin males show spontaneous paternal behaviors (Paternal), others display pup-directed aggression (Attackers). Here we took advantage of this phenotypic dichotomy and used RNA-sequencing in three important brain areas to characterize gene expression associated with paternal behaviors of Paternal males and compare it to experienced Fathers and Mothers. While Paternal males displayed the same range and extent of paternal behaviors as experienced Fathers, we observed structure-specific transcriptomic differences between parental behaviors phenotypes. Using differential expression, gene set expression, as well as co-expression network analyses, we found that phenotypic differences between Paternal males and Attackers were mainly reflected by the lateral septum (LS), and to a lower extent, the nucleus accumbens (NAc), transcriptomes. In the medial preoptic area (MPOA), the profiles of gene expression mainly reflected differences between females and males regardless of their parental behaviors phenotype. Functional enrichment analyses of those gene sets associated with Paternal males or Attackers in the LS and the NAc revealed the involvement of processes related to the mitochondria, RNA translation, protein degradation processes, as well as epigenetic regulation of gene expression. By leveraging the natural phenotypic differences in parental behaviors in virgin male prairie voles alongside fathers and mothers, we identified a marked structure- and phenotype-specific pattern of gene expression associated with spontaneous paternal behaviors independently from fatherhood and pair-bonding. The LS transcriptome related to the mitochondria, RNA translation, and protein degradation processes was thus highlighted as a primary candidate associated with the spontaneous display of paternal behaviors. Altogether, our observations further characterize the behavioral and transcriptomic signature of parental behaviors in the socially monogamous prairie vole and lay the groundwork to further our understanding of the molecular underpinnings of paternal behavior. The online version contains supplementary material available at 10.1186/s12864-022-08912-y.
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