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. 2024 Aug:62:91-103.
doi: 10.1016/j.jare.2023.09.015. Epub 2023 Sep 20.

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

Jianbo Yuan  1 , Xiaojun Zhang  1 , Xiaoxi Zhang  2 , Yamin Sun  3 , Chengzhang Liu  1 , Shihao Li  1 , Yang Yu  1 , Chengsong Zhang  1 , Songjun Jin  1 , Min Wang  4 , Jianhai Xiang  5 , Fuhua Li  6
Affiliations

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

Jianbo Yuan et al. J Adv Res. 2024 Aug.

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.

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Conflict of interest statement

Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Figures

None
Graphical abstract
Fig. 1
Fig. 1
Comparative genomic analyses of barnacles and their relatives. (A) The phylogenetic placement of barnacles in the arthropod phylogenetic tree. The numbers on the branches indicate the number of gene gains (+) or losses (-). The estimated divergence times are displayed below the phylogenetic tree. (B) The network plot of the functional enrichment of the expanded gene families. Each node in the plot indicates a KEGG pathway, and the color indicates the enrichment factor (fdr/p value). The node size indicates the number of genes involved in the corresponding pathway. Abbreviations: WGD, whole-genome duplication; MRCA, most recent common ancestor.
Fig. 2
Fig. 2
The interchromosomal synteny of C. mitella and P. pollicipes. (A) The interchromosomal synteny of C. mitella. (B) The interchromosomal synteny of P. pollicipes. A schematic representation of the genomic characteristics of the two barnacle genomes including (from the outer circle to inner circle): Track 1, 16 chromosomes of the genome; Track 2, protein-coding genes present on the scaffolds, where red represents genes on the forward strand and green represents genes on the reverse strand; Track 3, distribution of the gene density with sliding windows of 1 Mb, where a higher density is indicated by darker red; Track 4, distribution of the GC content in the genome; Track 5, schematic representation of the interchromosomal synteny of the two barnacle genomes, where the arc line indicates the major interchromosomal syntenic blocks in the C. mitella genome and the pairwise best hit homologous genes in the P. pollicipes genome. (C) The conserved synteny blocks between C. mitella and P. pollicipes. The red lines indicate the ohnologs of the four chromosomes (two paralogous chromosomes originating from the WGD event for C. mitella and P. pollicipes each). The gray lines indicate the ohnologs of the two paralogous/orthologous chromosomes that were not shared with the other two chromosomes.
Fig. 3
Fig. 3
The Hox gene cluster of ten arthropods. The boxes linked with a straight line indicate the ordered genes located on a single scaffold or pseudochromosome. The boxes with dotted lines indicate pseudogenes that could not be transcribed or translated. The images of various species were downloaded from the free silhouette images of PHYLOPIC (https://phylopic.org/).
Fig. 4
Fig. 4
The distribution of the synonymous substitution rate (Ks) of homologous gene groups for intraspecies and interspecies comparisons. The peaks in the light blue circle indicate the whole-genome duplication (WGD) events.
Fig. 5
Fig. 5
The differential expression patterns of the ohnologs during air exposure in barnacles. (A) The expression patterns of the ohnologs in a syntenic block of two paralogous chromosomes (Chr_14 and Chr_9) that originated from a whole-genome duplication (WGD) event (Fig. 2A). Individuals attached at high (H), medium (M), and low (L) elevation from sea level were sampled, and individuals that were exposed to seawater served as the controls (C). The lines that link two genes indicate that the two genes are ohnologs in the syntenic block. The genes encoding the broad-complex core protein (Br-C), longitudinals lacking protein (Lola), cytochrome P450 (P450), and zinc finger protein (ZFP) are involved in this syntenic block. The other genes are mostly encoding proteins with an unknown function. “*” indicates a significant differential expression in contrast to the control group (student t-test, p < 0.05). (B) The expression patterns of the ohnologs in a syntenic block of two paralogous chromosomes (Chr_5 and Chr_10) originated from a WGD event. The genes encoding ZFP, membrane metalloendopeptidase 1 (MMEL1), endothelin-converting enzyme (ECE), and BCL-6 corepressor (BCoR) are involved in this syntenic block.
Fig. 6
Fig. 6
Genes and metabolites involved in the intertidal adaptation of barnacles. (A) Volcano plot of differential metabolites between the controls (C) and medium elevation (M) groups of C. mitella . Red and green symbols represent significantly differentially regulated acyl-carnitines and FFAs during air exposure. (B) Schematic diagram of the accumulation of acyl-carnitines in C. mitella during air exposure. Green and red rounded rectangles represent significantly downregulated and upregulated metabolites, respectively. Blue and red rectangles represent the expression levels of the corresponding genes in the control group and the medium group, respectively.
Fig. 7
Fig. 7
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