Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, People's Republic of China.
University of Chinese Academy of Sciences, Beijing, People's Republic of China.
Proc Biol Sci. 2020 Feb 12;287(1920):20193008. doi: 10.1098/rspb.2019.3008.
Whole genome duplication (WGD) is commonly believed to play key roles in vertebrate evolution. However, nowadays polyploidy exists in a few fish, amphibian and reptile groups only, and seems to be an evolutionary dead end in vertebrates. We investigate the evolutionary significance of polyploidization in Cyprinidae-a fish family that contains more polyploid species than any other vertebrate group-with integrated biogeographic, phylogenetic and genomic analyses. First, polyploid species are found to be significantly frequent in areas of higher altitude and lower mean annual temperature compared with diploid species in Cyprinidae. Second, a polyploidy-related diversification rate shift is observed in Cyprinidae. This increased net diversification rate is only seen in three polyploid lineages, and other polyploid lineages have similar net diversification rate as well as diploid lineages in Cyprinidae. Interestingly, significant 'lag times' existed between polyploidization and radiation in Cyprinidae. Multiple polyploid lineages were established approximately 15 Ma through recurrent allopolyploidization events, but the net diversification rate did not start to increase until approximately 5 Ma-long after polyploidization events. Environmental changes associated with the continuous uplift of the Tibetan Plateau and climate change have probably promoted the initial establishment and subsequent radiation of polyploidy in Cyprinidae. Finally, the unique retention of duplicated genes in polyploid cyprinids adapted to harsh environments is found. Taken together, our results suggest that polyploidy in Cyprinidae is far more than an evolutionary dead end, but rather shows substantially adaptive potential. Polyploid cyprinids thus constitute an ideal model system for unveiling largely unexplored consequences of WGD in vertebrates, from genomic evolution to species diversification.
全基因组复制（WGD）被普遍认为在脊椎动物进化中发挥着关键作用。然而，如今多倍体仅存在于少数鱼类、两栖类和爬行类群体中，似乎是脊椎动物进化的死胡同。我们通过综合的生物地理、系统发育和基因组分析，研究了多倍体化在鲤科鱼类中的进化意义。首先，与鲤科鱼类中的二倍体物种相比，多倍体物种在高海拔和低年均温度地区的出现频率明显更高。其次，我们观察到了鲤科鱼类中与多倍体化相关的多样化率转变。这种净多样化率的增加仅见于三个多倍体谱系，而其他多倍体谱系与鲤科鱼类中的二倍体谱系具有相似的净多样化率。有趣的是，鲤科鱼类中的多倍体化与辐射之间存在显著的“滞后时间”。大约在 1500 万年前，通过反复的异源多倍体化事件建立了多个多倍体谱系，但直到大约 500 万年前，净多样化率才开始增加，这一时期远在多倍体化事件之后。与青藏高原持续抬升和气候变化相关的环境变化可能促进了鲤科鱼类多倍体的最初建立和随后的辐射。最后，我们发现多倍体鲤科鱼类中保留了大量适应恶劣环境的重复基因。总之，我们的研究结果表明，鲤科鱼类中的多倍体远非进化的死胡同，而是表现出了显著的适应潜力。因此，多倍体鲤科鱼类构成了揭示脊椎动物中全基因组复制的广泛未探索后果的理想模型系统，从基因组进化到物种多样化。
