Quantitative autistic traits are common, heritable, and continuously distributed across the general human population. Patterns of autistic traits within families suggest that more complex mechanisms than simple Mendelian inheritance—in particular, parent of origin effects—may be involved. The ideal strategy for ascertaining parent of origin effects is by half-sibling analysis, where half-siblings share one, but not both, parents and each individual belongs to a unique combination of paternal and maternal half-siblings. While this family structure is rare in humans, many of our primate relatives, including rhesus macaques, have promiscuous breeding systems that consistently produce paternal and maternal half-siblings for a given index animal. Rhesus macaques, like humans, also exhibit pronounced variation in social functioning. Here we assessed differential paternal versus maternal inheritance of social functioning in male rhesus macaque offspring (N = 407) using ethological observations and ratings on a reverse-translated quantitative autistic trait measurement scale. Restricted Maximum Likelihood mixed models with unbounded variance estimates were used to estimate the variance components needed to calculate the genetic contribution of parents as the proportion of phenotypic variance (σ2P) between sons that could uniquely be attributed to their shared genetics (σ2g), expressed as σ2g/σ2P (or the proportion of phenotypic variance attributable to genetic variance), as well as narrow sense heritability (h2). Genetic contributions and heritability estimates were strong and highly significant for sons who shared a father but weak and non-significant for sons who shared a mother. Importantly, these findings were detected using the same scores from the same sons in the same analysis, confirmed when paternal and maternal half-siblings were analyzed separately, and observed with two methodologically distinct behavioral measures. Finally, genetic contributions were similar for full-siblings versus half-siblings that shared only a father, further supporting a selective paternal inheritance effect. These data are correlational by nature. A larger sample that includes female subjects, enables deeper pedigree assessments, and supports molecular genetic analyses is warranted. Rhesus macaque social functioning may be paternally, but not maternally, inherited by sons. With continued investigation, this approach may yield important insights into sex differences in autism’s genetic liability.

中文翻译：

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恒河猴的社会功能是父系而非母系的，由儿子遗传：对自闭症的潜在影响

自闭症的数量特征是常见的、可遗传的，并且持续分布在整个人群中。家庭内自闭症特征的模式表明，可能涉及比简单的孟德尔遗传更复杂的机制，特别是父母的起源效应。确定起源父母影响的理想策略是通过同父异母兄弟姐妹分析，其中同父异母兄弟姐妹共享一个而非两个父母，并且每个人都属于父亲和母亲同父异母兄弟姐妹的独特组合。虽然这种家族结构在人类中很少见，但我们的许多灵长类亲戚，包括恒河猴，都拥有混杂的繁殖系统，不断为给定的指标动物产生父系和母系同父异母的兄弟姐妹。恒河猴和人类一样，在社会功能上也表现出明显的差异。在这里，我们使用行为学观察和反向翻译定量自闭症特征测量量表的评级，评估了雄性恒河猴后代（N = 407）社会功能的父系与母系遗传差异。使用具有无界方差估计的限制最大似然混合模型来估计计算父母遗传贡献所需的方差分量，作为儿子之间可唯一归因于其共同遗传 (σ2g) 的表型方差 (σ2P) 的比例，表示为σ2g/σ2P（或归因于遗传方差的表型方差的比例），以及狭义遗传力（h2）。对于有共同父亲的儿子来说，遗传贡献和遗传力估计很强并且非常显着，但对于有共同母亲的儿子来说，遗传贡献和遗传力估计很弱并且不显着。重要的是，这些发现是在同一分析中使用来自同一儿子的相同分数检测到的，在分别分析父亲和母亲同父异母兄弟姐妹时得到证实，并通过两种方法上不同的行为测量进行观察。最后，全兄弟姐妹和仅拥有父亲的同父异母兄弟姐妹的遗传贡献相似，进一步支持了选择性父系遗传效应。这些数据本质上是相关的。需要包括女性受试者在内的更大样本，以实现更深入的谱系评估，并支持分子遗传分析。恒河猴的社会功能可能是由儿子遗传的，但不是母系的。随着持续的研究，这种方法可能会对自闭症遗传倾向的性别差异产生重要的见解。