Genome-wide analysis reveals the contributors to fast molecular evolution of the Chinese hook snout carp (Opsariichthys bidens)

TL;DR

This study finds that the Chinese hook snout carp has unusually fast molecular evolution driven by ancestral traits and natural selection, with implications for understanding evolutionary mechanisms.

Contribution

The study identifies genome-wide contributors to fast molecular evolution in a fish species, linking it to ancestral states, adaptive selection, and gene-specific metabolic effects.

Findings

O. bidens has a significantly higher substitution rate and more fast-evolving genes compared to other fish species.

Adaptive selection, not random drift, explains most fast-evolving genes in O. bidens and related species.

Metabolic rate influences substitution rate in a gene-specific manner.

Abstract

Variations in molecular evolutionary rate have been widely investigated among lineages and genes. However, it remains an open question whether fast rate of molecular evolution is driven by natural selection or random drift, and how the fast rate is linked to metabolic rate. Additionally, previous studies on fast molecular evolution have been largely restricted to concatenated matrix of genes or a few specifically selected genes, but less is known for individual genes at the genome-wide level. Here we addressed these questions using more than 5000 single-copy orthologous (SCO) genes through comparative genomic and phylogenetic analyses among fishes, with a special focus on a newly-sequenced clupeocephalan fish the Chinese hook snout carp Opsariichthys bidens. We showed O. bidens displays significantly higher mean substitution rate and more fast-evolving SCO genes (2172 genes) than most fishes studied here. The rapidly evolving genes are enriched in highly conserved and very basic functions such as translation and ribosome that are critical for biological fitness. We further revealed that ∼25 % of these fast-evolving genes exhibit a constant increase of substitution rate from the common ancestor down to the present, suggesting a neglected but important contribution from ancestral states. Model fitting showed that ∼85 % of fast-evolving genes exclusive to O. bidens and related species follow the adaptive evolutionary model rather than random-drift model, and 7.6 % of fast-evolving genes identified in O. bidens have experienced positive selection, both indicating the reflection of adaptive selection. Finally, metabolic rate was observed to be linked with substitution rate in a gene-specific manner. Overall, our findings reveal fast molecular evolution of SCO genes at genome-wide level in O. bidens, and uncover the evolutionary and ecological contributors to it.

ga1

•We sequenced the chromosome-level genome of the Chinese hook snout carp Opsariichthys bidens.•O. bidens displays higher substitution rate and more fast-evolving genes than most of other fish species studied here.•The ancestral state contributed to the fast molecular evolution, and the underlying molecular mechanism was suggested.•Adaptive selection rather than random drift acts as another important contributor to the fast molecular evolution.•Effect of metabolic rate on substitution rate is gene-specific, shedding light on previous contradictory observations.

We sequenced the chromosome-level genome of the Chinese hook snout carp Opsariichthys bidens.

O. bidens displays higher substitution rate and more fast-evolving genes than most of other fish species studied here.

The ancestral state contributed to the fast molecular evolution, and the underlying molecular mechanism was suggested.

Adaptive selection rather than random drift acts as another important contributor to the fast molecular evolution.

Effect of metabolic rate on substitution rate is gene-specific, shedding light on previous contradictory observations.

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