Population genomics of an icefish reveals mechanisms of glacier-driven adaptive radiation in Antarctic notothenioids

Abstract Background Antarctica harbors the bulk of the species diversity of the dominant teleost fish suborder—Notothenioidei. However, the forces that shape their evolution are still under debate. Results We sequenced the genome of an icefish, Chionodraco hamatus, and used population genomics and d...

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Bibliographic Details
Published in:BMC Biology
Main Authors: Ying Lu, Wenhao Li, Yalin Li, Wanying Zhai, Xuming Zhou, Zhichao Wu, Shouwen Jiang, Taigang Liu, Huamin Wang, Ruiqin Hu, Yan Zhou, Jun Zou, Peng Hu, Guijun Guan, Qianghua Xu, Adelino V. M. Canário, Liangbiao Chen
Format: Article in Journal/Newspaper
Language:English
Published: BMC 2022
Subjects:
Kya
Online Access:https://doi.org/10.1186/s12915-022-01432-x
https://doaj.org/article/d40c2200b8254c7692b93bf700ec2acf
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Summary:Abstract Background Antarctica harbors the bulk of the species diversity of the dominant teleost fish suborder—Notothenioidei. However, the forces that shape their evolution are still under debate. Results We sequenced the genome of an icefish, Chionodraco hamatus, and used population genomics and demographic modelling of sequenced genomes of 52 C. hamatus individuals collected mainly from two East Antarctic regions to investigate the factors driving speciation. Results revealed four icefish populations with clear reproduction separation were established 15 to 50 kya (kilo years ago) during the last glacial maxima (LGM). Selection sweeps in genes involving immune responses, cardiovascular development, and photoperception occurred differentially among the populations and were correlated with population-specific microbial communities and acquisition of distinct morphological features in the icefish taxa. Population and species-specific antifreeze glycoprotein gene expansion and glacial cycle-paced duplication/degeneration of the zona pellucida protein gene families indicated fluctuating thermal environments and periodic influence of glacial cycles on notothenioid divergence. Conclusions We revealed a series of genomic evidence indicating differential adaptation of C. hamatus populations and notothenioid species divergence in the extreme and unique marine environment. We conclude that geographic separation and adaptation to heterogeneous pathogen, oxygen, and light conditions of local habitats, periodically shaped by the glacial cycles, were the key drivers propelling species diversity in Antarctica.