Chen Jenny, Richardson Phoebe R, Kirby Christopher, Eddy Sean R, Hoekstra Hopi E
Department of Molecular & Cellular Biology, Harvard University, Cambridge, United States.
Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States.
Elife. 2025 Apr 7;13:RP103109. doi: 10.7554/eLife.103109.
Genetic variation is known to contribute to the variation of animal social behavior, but the molecular mechanisms that lead to behavioral differences are still not fully understood. Here, we investigate the cellular evolution of the hypothalamic preoptic area (POA), a brain region that plays a critical role in social behavior, across two sister species of deer mice ( and ) with divergent social systems. These two species exhibit large differences in mating and parental care behavior across species and sex. Using single-nucleus RNA-sequencing, we build a cellular atlas of the POA for males and females of both species. We identify four cell types that are differentially abundant across species, two of which may account for species differences in parental care behavior based on known functions of these cell types. Our data further implicate two sex-biased cell types to be important for the evolution of sex-specific behavior. Finally, we show a remarkable reduction of sex-biased gene expression in , a monogamous species that also exhibits reduced sexual dimorphism in parental care behavior. Our POA atlas is a powerful resource to investigate how molecular neuronal traits may be evolving to give rise to innate differences in social behavior across animal species.
已知基因变异会导致动物社会行为的差异，但其导致行为差异的分子机制仍未完全明确。在此，我们研究了鹿鼠两个姐妹物种（和）下丘脑视前区（POA）的细胞进化，该脑区在社会行为中起着关键作用，这两个物种具有不同的社会系统。这两个物种在跨物种和性别的交配及亲代抚育行为上表现出巨大差异。通过单核RNA测序，我们构建了这两个物种雄性和雌性POA的细胞图谱。我们鉴定出四种在物种间丰度有差异的细胞类型，其中两种基于这些细胞类型的已知功能，可能解释了亲代抚育行为的物种差异。我们的数据进一步表明，两种性别偏向性细胞类型对性别特异性行为的进化很重要。最后，我们发现，在一个实行一夫一妻制且在亲代抚育行为中也表现出性二态性降低的物种中，性别偏向性基因表达显著减少。我们的POA图谱是一个强大的资源，可用于研究分子神经元特征如何进化，从而导致动物物种间社会行为的固有差异。
