Dynamic evolution of transposable elements, demographic history, and gene content of paleognathous birds

Zool Res. 2021 Jan 18;42(1):51-61. doi: 10.24272/j.issn.2095-8137.2020.175.

Abstract

Palaeognathae includes ratite and tinamou species that are important for understanding early avian evolution. Here, we analyzed the whole-genome sequences of 15 paleognathous species to infer their demographic histories, which are presently unknown. We found that most species showed a reduction of population size since the beginning of the last glacial period, except for those species distributed in Australasia and in the far south of South America. Different degrees of contraction and expansion of transposable elements (TE) have shaped the paleognathous genome architecture, with a higher transposon removal rate in tinamous than in ratites. One repeat family, AviRTE, likely underwent horizontal transfer from tropical parasites to the ancestor of little and undulated tinamous about 30 million years ago. Our analysis of gene families identified rapid turnover of immune and reproduction-related genes but found no evidence of gene family changes underlying the convergent evolution of flightlessness among ratites. We also found that mitochondrial genes have experienced a faster evolutionary rate in tinamous than in ratites, with the former also showing more degenerated W chromosomes. This result can be explained by the Hill-Robertson interference affecting genetically linked W chromosomes and mitochondria. Overall, we reconstructed the evolutionary history of the Palaeognathae populations, genes, and TEs. Our findings of co-evolution between mitochondria and W chromosomes highlight the key difference in genome evolution between species with ZW sex chromosomes and those with XY sex chromosomes.

古颚类鸟类包括平胸目和䳍形目,对它们的研究有助于我们对鸟类早期演化的了解。我们通过对古颚类15个物种全基因组序列的分析来重构其种群演化历史。除了分布在澳大利亚,新西兰和南美洲最南端的物种,我们发现,自上个冰川期开始以来,大多数古鄂类物种的种群数量都减少了。基因组转座元件不同程度的收缩和扩增塑造了古颚类的基因组结构,相对于平胸目,䳍形目的转座子有更高的丢失速率。大约3000万年前,AviRTE重复序列可能发生了从热带寄生虫向小穴䳍和波斑穴䳍祖先的水平转移。我们对基因家族的分析确定了与免疫和繁殖相关基因的快速变化,但是没有发现平胸目飞行趋同退化的基因家族变化。我们还发现线粒体基因在䳍形目中的进化速率高于平胸目,前者的W染色体退化地更严重。该结果可以通过W染色体和线粒体因为遗传连锁受到希尔·罗伯森干涉效应的影响来解释。综上,我们重建了古颚类种群,基因和转座元件的演化历史。线粒体和W染色体共同演化的发现突出了ZW性染色体物种与XY性染色体物种之间基因组进化的关键差异。.

Keywords: Demographic history; Gene families; Mitochondria; Paleognaths; Transposable elements.

MeSH terms

  • Animals
  • Biological Evolution*
  • Birds / genetics*
  • DNA Transposable Elements / genetics*
  • DNA, Mitochondrial / genetics
  • Female
  • Male
  • Multigene Family
  • Sex Chromosomes / genetics
  • Time Factors

Substances

  • DNA Transposable Elements
  • DNA, Mitochondrial

Grants and funding

This study was supported by the National Natural Science Foundation of China (31671319, 31722050, 32061130208), Natural Science Foundation of Zhejiang Province (LD19C190001), and European Research Council Starting Grant (grant agreement 677696) to Q.Z.; the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB31020000, XDB13000000), International Partnership Program of Chinese Academy of Sciences (152453KYSB20170002), Carlsberg Foundation (CF16-0663), and Villum Foundation (25900) to G.J.Z.