Large-scale sequencing of flatfish genomes provides insights into the polyphyletic origin of their specialized body plan

Jianshe Zhang,Wei Shi,Shunping He,Liang Zhu,Yan Zeng,Chen Zhang,Yanli Qin,Wen Wang,Li Gong,Zhen-Ming Lü ,Yifan Wang,Zhenzhu Li,Yongxin Li,Wenting Wan,Zhongkai Wang,Haifeng Jiang,Xianqing Chen,Bingyu Mao,Yongjiu Chen,Yandong Ren,Haorong Li,Liqin Liu,Kun Wang,Xiaoyu Kong,Hairong Luo,Hui Jiang

doi:10.1038/s41588-021-00836-9

Abstract

The evolutionary and genetic origins of the specialized body plan of flatfish are largely unclear. We analyzed the genomes of 11 flatfish species representing 9 of the 14 Pleuronectiforme families and conclude that Pleuronectoidei and Psettodoidei do not form a monophyletic group, suggesting independent origins from different percoid ancestors. Genomic and transcriptomic data indicate that genes related to WNT and retinoic acid pathways, hampered musculature and reduced lipids might have functioned in the evolution of the specialized body plan of Pleuronectoidei. Evolution of Psettodoidei involved similar but not identical genes. Our work provides valuable resources and insights for understanding the genetic origins of the unusual body plan of flatfishes.

Highlights

The colonization of the seafloor is one of the most important events in evolutionary history, which led to an explosive radiation and large-scale morphological diversification of marine phyla[1,2]
All these studies mainly focused on the asymmetric body plan in flatfishes under the framework of only one or two flatfish species, while the genetic basis of a wider spectrum of morphological adaptations in the whole flatfish group remains to be explored from a systematic evolutionary perspective
Similar to what was observed in real flatfish Pleuronectoidei’ (RFP), we found the DGC component gene[82] and lipogenesis-related genes[83,84,85,86] to be rapidly evolving in flatfish-like Psettodoidei’ (FLP), in bbox[1] (REGs, P = 8.75 × 10−6) and mex3c (REGs, P = 1.20 × 10−5) (Supplementary Table 91 and Supplementary Note 20)

Summary

Introduction

The colonization of the seafloor is one of the most important events in evolutionary history, which led to an explosive radiation and large-scale morphological diversification of marine phyla[1,2]. Shao et al.[19] were the first to elaborate on this topic by applying a genomic framework and providing evidence for retinoic acid (RA) and TH involvement in the regulation of body plan asymmetry of flatfishes All these studies mainly focused on the asymmetric body plan in flatfishes under the framework of only one or two flatfish species, while the genetic basis of a wider spectrum of morphological adaptations (for example, body-plan flatness, body and eye asymmetry and fin modification) in the whole flatfish group remains to be explored from a systematic evolutionary perspective. Articles chatareus and 2 from two tissues of Polydactylus sextarius) that we generated, we systematically studied: (1) the phylogeny of flatfishes, which provides an evolutionary framework for better understanding the genetic adaptation of flatfishes; and (2) genes that experienced significant alterations, to gain insights into the genetic basis underlying the unusual body plan of flatfishes

Methods

Results

Conclusion