Decelerated genome evolution in modern vertebrates revealed by analysis of multiple lancelet genomes.

Shengfeng Huang,Meiling Dong,Ruihua Wang,Jie Li,Guang Li,Hongchen Zhao,Zelin Chen,Anlong Xu,Sisi Zhou,Shangwu Chen,Yonggui Fu,Yiquan Wang,Leiming You,Xinyu Yan,Qingyu Yan,Ting Yu,Qiujin Zhang,Fenfang Wu,Rui Li,Guangrui Huang,Xin Tao,Shaochun Yuan,Ping-Shih Yang ,Tao Deng ,Pierre Pontarotti

doi:10.1038/ncomms6896

Abstract

Vertebrates diverged from other chordates ~500 Myr ago and experienced successful innovations and adaptations, but the genomic basis underlying vertebrate origins are not fully understood. Here we suggest, through comparison with multiple lancelet (amphioxus) genomes, that ancient vertebrates experienced high rates of protein evolution, genome rearrangement and domain shuffling and that these rates greatly slowed down after the divergence of jawed and jawless vertebrates. Compared with lancelets, modern vertebrates retain, at least relatively, less protein diversity, fewer nucleotide polymorphisms, domain combinations and conserved non-coding elements (CNE). Modern vertebrates also lost substantial transposable element (TE) diversity, whereas lancelets preserve high TE diversity that includes even the long-sought RAG transposon. Lancelets also exhibit rapid gene turnover, pervasive transcription, fastest exon shuffling in metazoans and substantial TE methylation not observed in other invertebrates. These new lancelet genome sequences provide new insights into the chordate ancestral state and the vertebrate evolution.

Highlights

Vertebrates diverged from other chordates B500 Myr ago and experienced successful innovations and adaptations, but the genomic basis underlying vertebrate origins are not fully understood
We reasoned that haplotypes could be better resolved using longer reads, whereas base-level errors could be rectified by a high depth of short reads
We discovered thousands of coding exon rearrangements between the two lancelet species, a frequency that is 2- to 100-fold higher than that observed in vertebrates, urochordates and other investigated animals (Fig. 6a; Supplementary Table 24; Supplementary Note 13)

Summary

Introduction

Vertebrates diverged from other chordates B500 Myr ago and experienced successful innovations and adaptations, but the genomic basis underlying vertebrate origins are not fully understood. Lancelets exhibit rapid gene turnover, pervasive transcription, fastest exon shuffling in metazoans and substantial TE methylation not observed in other invertebrates. These new lancelet genome sequences provide new insights into the chordate ancestral state and the vertebrate evolution. We generate 14 transcriptomes representing different developmental stages, tissues and immune responses and carried out whole-genome resequencing and bisulfite sequencing of five additional individuals. Combining these new data with the Florida lancelet draft genome, we reevaluate the evolutionary rates of different genetic events within lancelets and among major chordate lineages. The new information reveals the genomic features that may have driven the origin and subsequent evolution of vertebrates

Methods

Results

Conclusion