Chen Jian-Hai, Landback Patrick, Arsala Deanna, Guzzetta Alexander, Xia Shengqian, Atlas Jared, Sosa Dylan, Zhang Yong E, Cheng Jingqiu, Shen Bairong, Long Manyuan
Department of Ecology and Evolution, The University of Chicago, 1101 E 57th Street, Chicago, IL 60637.
Institutes for Systems Genetics, West China University Hospital, Chengdu 610041, China.
bioRxiv. 2024 Sep 4:2023.11.14.567139. doi: 10.1101/2023.11.14.567139.
New genes (or young genes) are genetic novelties pivotal in mammalian evolution. However, their phenotypic impacts and evolutionary patterns over time remain elusive in humans due to the technical and ethical complexities of functional studies. Integrating gene age dating with Mendelian disease phenotyping, our research shows a gradual rise in disease gene proportion as gene age increases. Logistic regression modeling indicates that this increase in older genes may be related to their longer sequence lengths and higher burdens of deleterious de novo germline variants (DNVs). We also find a steady integration of new genes with biomedical phenotypes into the human genome over macroevolutionary timescales (~0.07% per million years). Despite this stable pace, we observe distinct patterns in phenotypic enrichment, pleiotropy, and selective pressures across gene ages. Notably, young genes show significant enrichment in diseases related to the male reproductive system, indicating strong sexual selection. Young genes also exhibit disease-related functions in tissues and systems potentially linked to human phenotypic innovations, such as increased brain size, musculoskeletal phenotypes, and color vision. We further reveal a logistic growth pattern of pleiotropy over evolutionary time, indicating a diminishing marginal growth of new functions for older genes due to intensifying selective constraints over time. We propose a "pleiotropy-barrier" model that delineates higher potentials for phenotypic innovation in young genes compared to older genes, a process that is subject to natural selection. Our study demonstrates that evolutionarily new genes are critical in influencing human reproductive evolution and adaptive phenotypic innovations driven by sexual and natural selection, with low pleiotropy as a selective advantage.
新基因(或年轻基因)是哺乳动物进化中的关键遗传新奇事物。然而,由于功能研究的技术和伦理复杂性,它们在人类中的表型影响和随时间的进化模式仍然难以捉摸。通过将基因年龄测定与孟德尔疾病表型分析相结合,我们的研究表明,随着基因年龄的增加,疾病基因的比例逐渐上升。逻辑回归模型表明, older genes的这种增加可能与其较长的序列长度和较高的有害新生种系变异(DNV)负担有关。我们还发现在宏观进化时间尺度上(约每百万年0.07%),新基因与生物医学表型稳定地整合到人类基因组中。尽管这个速度很稳定,但我们观察到不同基因年龄在表型富集、多效性和选择压力方面存在明显模式。值得注意的是,年轻基因在与雄性生殖系统相关的疾病中显著富集,表明存在强烈的性选择。年轻基因在可能与人类表型创新相关的组织和系统中也表现出与疾病相关的功能,如脑容量增加、肌肉骨骼表型和色觉。我们进一步揭示了多效性在进化时间上的逻辑增长模式,表明由于随着时间的推移选择约束加剧, older genes新功能的边际增长逐渐减少。我们提出了一个“多效性障碍”模型,该模型描述了与 older genes相比,年轻基因在表型创新方面具有更高的潜力,这一过程受自然选择的影响。我们的研究表明,进化上新基因在影响人类生殖进化以及由性选择和自然选择驱动的适应性表型创新方面至关重要,低多效性是一种选择优势。