Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, 100101 Beijing, China.
University of Chinese Academy of Sciences, 100049 Beijing, China.
Mol Biol Evol. 2024 Nov 1;41(11). doi: 10.1093/molbev/msae221.
Whole-genome duplication (WGD), or polyploidization, is a major contributor to biodiversity. However, the establishment and survival of WGDs are often considered to be stochastic, since elucidating the processes of WGD establishment remains challenging. In the current study, we explored the processes leading to polyploidy establishment in snow carp (Cyprinidae: Schizothoracinae), a predominant component of the ichthyofauna of the Tibetan Plateau and its surrounding areas. Using large-scale genomic data from isoform sequencing, we analyzed ohnolog genealogies and divergence in hundreds to thousands of gene families across major snow carp lineages. Our findings demonstrated that independent autopolyploidization subsequent to speciation was prevalent, while autopolyploidization followed by speciation also occurred in the diversification of snow carp. This was further supported by matrilineal divergence and drainage evolution evidence. Contrary to the long-standing hypothesis that ancient polyploidization preceded the diversification of snow carp, we determined that polyploidy in extant snow carp was established by recurrent autopolyploidization events during the Pleistocene. These findings indicate that the diversification of extant snow carp resembles a coordinated duet: first, the uplift of the Tibetan Plateau orchestrated the biogeography and diversification of their diploid progenitors; then, the extensive Pliocene-Pleistocene climate changes acted as relay runners, further fueling diversification through recurrent autopolyploidization. Overall, this study not only reveals a hitherto unrecognized recent WGD lineage in vertebrates but also advances current understanding of WGD processes, emphasizing that WGD establishment is a nonstochastic event, emerging from numerous adaptations to environmental challenges and recurring throughout evolutionary history rather than merely in plants.
全基因组复制（WGD）或多倍体化是生物多样性的主要贡献者。然而，WGD 的建立和存活通常被认为是随机的，因为阐明 WGD 建立的过程仍然具有挑战性。在本研究中，我们探索了导致青藏高原及其周边地区主要鱼类雪鲤鱼（鲤科：裂腹鱼科）多倍体建立的过程。我们使用来自异构体测序的大规模基因组数据，分析了数百到数千个基因家族的同源基因谱系和分化。我们的研究结果表明，独立的种内同源多倍化随后发生是普遍的，而在雪鲤鱼的多样化过程中也发生了种内同源多倍化随后发生的情况。这进一步得到了母系分化和水系演化证据的支持。与古代多倍体化先于雪鲤鱼多样化的长期假说相反，我们确定了现存雪鲤鱼的多倍体是在更新世通过反复的种内同源多倍化事件建立的。这些发现表明，现存雪鲤鱼的多样化类似于协调的二重奏：首先，青藏高原的隆起协调了它们的二倍体祖先的生物地理学和多样化；然后，广泛的上新世-更新世气候变化作为接力赛跑者，通过反复的种内同源多倍化进一步推动了多样化。总的来说，这项研究不仅揭示了脊椎动物中一个以前未被认识到的近期 WGD 谱系，而且还推进了对 WGD 过程的理解，强调了 WGD 建立是一个非随机事件，它是从对环境挑战的无数适应中产生的，并且在进化历史中反复出现，而不仅仅是在植物中。
