The genome of Nautilus pompilius illuminates eye evolution and biomineralization

Yang Zhang,He Dai,Mingli Ma,Minwei Huang,Haitao Ma,Huawei Mu,Nai-Kei Wong,Yuanyan Xiong,Zhiming Xiang,Lvping Zhang,Fan Mao,Jun Li,Fan Wang,Oleg Simakov,Xiyu Mu,Yuehuan Zhang,Xiaoyuan Song,Hongkun Zheng,Ziwei Zhang,Shijun Xiao ,Lili Wang,Yongbo Bao,Yu Zhou

doi:10.1038/s41559-021-01448-6

Abstract

Nautilus is the sole surviving externally shelled cephalopod from the Palaeozoic. It is unique within cephalopod genealogy and critical to understanding the evolutionary novelties of cephalopods. Here, we present a complete Nautilus pompilius genome as a fundamental genomic reference on cephalopod innovations, such as the pinhole eye and biomineralization. Nautilus shows a compact, minimalist genome with few encoding genes and slow evolutionary rates in both non-coding and coding regions among known cephalopods. Importantly, multiple genomic innovations including gene losses, independent contraction and expansion of specific gene families and their associated regulatory networks likely moulded the evolution of the nautilus pinhole eye. The conserved molluscan biomineralization toolkit and lineage-specific repetitive low-complexity domains are essential to the construction of the nautilus shell. The nautilus genome constitutes a valuable resource for reconstructing the evolutionary scenarios and genomic innovations that shape the extant cephalopods.

Highlights

Nautilus is the sole surviving externally shelled cephalopod from the Palaeozoic
Our analyses reveal that the nautilus genome is the smallest when compared to published genomes of coleoid cephalopods; it contains the least number of encoding genes and hitherto the lowest evolutionary rate in the group
Comparative analysis further revealed that the make-up of transposable elements (TEs) in N. pompilius is strikingly different to coleoid lineages (Fig. 1a and Supplementary Table 4)

Summary

Introduction

Nautilus is the sole surviving externally shelled cephalopod from the Palaeozoic It is unique within cephalopod genealogy and critical to understanding the evolutionary novelties of cephalopods. We present a complete Nautilus pompilius genome as a fundamental genomic reference on cephalopod innovations, such as the pinhole eye and biomineralization. Multiple genomic innovations including gene losses, independent contraction and expansion of specific gene families and their associated regulatory networks likely moulded the evolution of the nautilus pinhole eye. Genomic sequencing efforts in coleoids revealed that specific gene family expansions and genome rearrangements may drive the evolution of morphological novelties in these organisms[9,10,11,12]. Comparative genomics analysis revealed that co-evolution of gene losses and gene family contraction are associated with pinhole eye formation in nautilus, suggesting plausible degeneration from a more complex. Lineage-specific expansion of gene families implicates the active operation of distinct evolutionary strategies of innate immune defence in different cephalopods

Methods

Results

Conclusion