An ancient whole-genome duplication in barnacles contributes to their diversification and intertidal sessile life adaptation

Jianbo Yuan; Xiaojun Zhang; Xiaoxi Zhang; Yamin Sun; Chengzhang Liu; Shihao Li; Yang Yu; Chengsong Zhang; Songjun Jin; Min Wang; Jianhai Xiang; Fuhua Li

doi:10.1016/j.jare.2023.09.015

An ancient whole-genome duplication in barnacles contributes to their diversification and intertidal sessile life adaptation

J Adv Res. 2023 Sep 20:S2090-1232(23)00264-3. doi: 10.1016/j.jare.2023.09.015. Online ahead of print.

Authors

Jianbo Yuan¹, Xiaojun Zhang¹, Xiaoxi Zhang², Yamin Sun³, Chengzhang Liu¹, Shihao Li¹, Yang Yu¹, Chengsong Zhang¹, Songjun Jin¹, Min Wang⁴, Jianhai Xiang⁵, Fuhua Li⁶

Affiliations

¹ CAS and Shandong Province Key Laboratory of Experimental Marine Biology, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China.
² CAS and Shandong Province Key Laboratory of Experimental Marine Biology, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China.
³ Research Center for Functional Genomics and Biochip, Tianjin 300457, China.
⁴ TEDA Institute of Biological Sciences and Biotechnology, Nankai University, Tianjin 300457, China; Key Laboratory of Molecular Microbiology and Technology, Ministry of Education, Nankai University, Tianjin 300071, China. Electronic address: wangm@nankai.edu.cn.
⁵ CAS and Shandong Province Key Laboratory of Experimental Marine Biology, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China. Electronic address: jhxiang@qdio.ac.cn.
⁶ CAS and Shandong Province Key Laboratory of Experimental Marine Biology, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China. Electronic address: fhli@qdio.ac.cn.

PMID: 37734567
DOI: 10.1016/j.jare.2023.09.015

Abstract

Introduction: Whole-genome duplication (WGD) is one of the most sudden and dramatic events rarely reported in invertebrates, but its occurrence can lead to physiological, morphological, and behavioral diversification. WGD has also never been reported in barnacles, which is one of the most unique groups of crustaceans with extremely speciallized morphology (calcareous shells) and habits (intertidal sessile lifestyle).

Objectives: To investigate whether WGD has occurred in barnacles and examine its potential role in driving the adaptive evolution and diversification of barnacles.

Methods: Based on a newly sequenced and assembled chromosome-level barnacle genome, a novel WGD event has been identified in barnacles through a comprehensive analysis of interchromosomal synteny, the Hox gene cluster, and synonymous substitution distribution.

Results: We provide ample evidences for WGD in the barnacle genomes. Comparative genomic analysis indicates that this WGD event predates the divergence of Thoracicalcarea, occurring more than 247 million years ago. The retained ohnologs from the WGD are primarily enriched in various pathways related to environmental information processing, shedding light on the adaptive evolution and diversification of intertidal sessile lifestyle. In addition, transcriptomic analyses show that most of these ohnologs were differentially expressed following the ebb of tide. And the cytochrome P450 ohnologs with differential expression patterns are subject to subfunctionalization and/or neofunctionalization for intertidal adaptation. Besides WGD, parallel evolution underlying intertidal adaptation has also occurred in barnacles.

Conclusion: This study revealed an ancient WGD event in the barnacle genomes, which is potentially associated with the origin and diversification of thoracican barnacles, and may have contributed to the adaptive evolution of their intertidal sessile lifestyle.

Keywords: Barnacle genome; Comparative genomics; Intertidal adaptation; Transcriptome analysis; Whole-genome duplication.