Inventing monogamy: innovation and adaptation in the epigenome

新的行为是如何形成的？最近的技术进步使我们能够准确地询问哪些脱氧核糖核酸（DNA）序列是基因表达、神经功能和复杂行为的进化创新的基础。一个有机体与另一个个体建立联系的能力是一种复杂的行为，它塑造了包括人类在内的许多物种所表现出的社会行为。在目前的项目中，研究人员发现了一种被充分研究过的物种——一夫一妻制草原田鼠——社会联系的进化适应。研究人员比较了区分一夫一妻制草原田鼠和滥交亲戚的DNA序列的细微变化。他们还想知道，DNA的这些变化是否会影响大脑中对配对很重要的区域的基因功能，以及对空间记忆很重要的大脑区域，因为空间利用是动物交配系统的一个主要因素。最后，研究人员通过检查DNA变异的模式来询问自然选择是否对这些DNA序列起作用。这些发现将有助于理解复杂行为的变化是如何从DNA变异中产生的。为了完成研究，研究人员将从代表性不足的群体中招募和培训本科生。此外，研究人员将开发和传播对各种物种进行类似研究所需的研究工具，使对任何物种的基因组功能和行为进行前沿研究变得更加容易。从这项工作中获得的答案将阐明行为与导致多样性和疾病的微妙遗传变异之间的关系。一个基因型是如何被一个基因座一个基因座地塑造成一个新的表现型的？研究人员利用鼠属作为模型，在社会神经科学、分子遗传学和行为生态学的广泛工作基础上，理解导致社会一夫一妻制的表观遗传学创新。他们研究了三种田鼠的表观基因组及其进化：一夫一妻制的草原田鼠M. ochrogaster；滥交的草地田鼠（M. pennsylvanicus）；以及一个滥交的外群，加利福尼亚田鼠，加利福尼亚田鼠。尽管许多大脑区域值得研究，但研究人员主要关注四个大脑区域：奖励结构（伏隔核，腹侧苍白球）和空间记忆结构（海马体，脾后皮质）。在第一个目标中，他们使用RNA-seq和ChIP-seq来识别基因调控的物种差异。在第二个目标中，他们使用系统发育和群体遗传方法来识别表观基因组中的适应性。这两个数据集的交集将确定可能与配对键形成和交配系统空间认知差异有因果关系的调控区域。最后，研究人员测试了这一群体中一夫一妻制的进化是否主要依赖于与结合、认知或两者相关的变化。鉴定出的DNA序列可以在未来的研究中进行操作。

How do new behaviors evolve? Recent technical advances allow us to ask exactly which deoxyribonucleic acid (DNA) sequences underlie evolutionary innovations in gene expression, neural function, and complex behaviors. The ability of an organism to form a bond with another individual is a complex behavior, one that shapes the social behaviors exhibited by many species, including humans. In the current project, the investigators identify evolutionary adaptations that underlie social bonding in a well-studied species, the monogamous prairie vole. The investigators compare the subtle changes in DNA sequences that distinguish monogamous prairie voles from promiscuous relatives. They also ask whether these changes in DNA influence gene function in brain regions important for pair-bonding as well as brain regions important for spatial memory because space use is a major factor in animal mating systems. Lastly, the investigators ask whether natural selection has operated on these DNA sequences by examining patterns of DNA variation. The findings will help understand how changes in complex behavior can emerge from variation in DNA. To complete the studies, the investigators will recruit and train undergraduates from under-represented groups. Further, the investigators will develop and disseminate research tools needed to perform similar studies on a great variety of species, making it easier to do cutting-edge studies of genome function and behavior in any species. The answers obtained from this work will elucidate the relation between behavior and subtle genetic variations that contribute to diversity and disease.How is an existing genotype sculpted, locus by locus, to result in a new phenotype? The investigators use the genus Microtus as a model for understanding the epigenetic innovations that gave rise to social monogamy, building on an extensive body of work in social neuroscience, molecular genetics, and behavioral ecology. They examine the epigenome and its evolution in three vole species: the monogamous prairie vole, M. ochrogaster; the promiscuous meadow vole, M. pennsylvanicus; and a promiscuous outgroup, the California vole, M. californicus. Although many brain regions merit study, the investigators focus on four brain regions: reward structures (nucleus accumbens, ventral pallidum) and spatial memory structures (hippocampus, retrosplenial cortex). In the first aim, they use RNA-seq and ChIP-seq to identify species differences in gene regulation. In second aim, they use phylogenetic and population genetic methods to identify adaptations within the epigenome. The intersection of these two data sets will identify regulatory regions likely to be causally involved in pair-bond formation, and in mating system differences in spatial cognition. Finally, the investigators test whether the evolution of monogamy in this group relied predominantly on changes related to bonding, to cognition, or both. The identified DNA sequences can then be subject to manipulation in future studies.