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...
| Main Authors: | , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2022-10-01
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| Series: | BMC Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12915-022-01432-x |
| _version_ | 1817983872596443136 |
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| author | 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 |
| author_facet | 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 |
| author_sort | Ying Lu |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-13T23:38:20Z |
| format | Article |
| id | doaj.art-d40c2200b8254c7692b93bf700ec2acf |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-04-13T23:38:20Z |
| publishDate | 2022-10-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-d40c2200b8254c7692b93bf700ec2acf2022-12-22T02:24:37ZengBMCBMC Biology1741-70072022-10-0120112010.1186/s12915-022-01432-xPopulation genomics of an icefish reveals mechanisms of glacier-driven adaptive radiation in Antarctic notothenioidsYing Lu0Wenhao Li1Yalin Li2Wanying Zhai3Xuming Zhou4Zhichao Wu5Shouwen Jiang6Taigang Liu7Huamin Wang8Ruiqin Hu9Yan Zhou10Jun Zou11Peng Hu12Guijun Guan13Qianghua Xu14Adelino V. M. Canário15Liangbiao Chen16Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources (Ministry of Education), Shanghai Ocean UniversityKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources (Ministry of Education), Shanghai Ocean UniversityKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources (Ministry of Education), Shanghai Ocean UniversityKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources (Ministry of Education), Shanghai Ocean UniversityInstitute of Zoology, Chinese Academy of ScienceKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources (Ministry of Education), Shanghai Ocean UniversityKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources (Ministry of Education), Shanghai Ocean UniversityInternational Research Center for Marine Biosciences (Ministry of Science and Technology), Shanghai Ocean UniversityKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources (Ministry of Education), Shanghai Ocean UniversityKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources (Ministry of Education), Shanghai Ocean UniversityKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources (Ministry of Education), Shanghai Ocean UniversityKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources (Ministry of Education), Shanghai Ocean UniversityKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources (Ministry of Education), Shanghai Ocean UniversityKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources (Ministry of Education), Shanghai Ocean UniversityKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources (Ministry of Education), Shanghai Ocean UniversityInternational Research Center for Marine Biosciences (Ministry of Science and Technology), Shanghai Ocean UniversityKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources (Ministry of Education), Shanghai Ocean UniversityAbstract 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.https://doi.org/10.1186/s12915-022-01432-xQuaternary glacial cyclesSelection sweepReproductive isolationGut microbiotaAdaptive radiation |
| spellingShingle | 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 Population genomics of an icefish reveals mechanisms of glacier-driven adaptive radiation in Antarctic notothenioids BMC Biology Quaternary glacial cycles Selection sweep Reproductive isolation Gut microbiota Adaptive radiation |
| title | Population genomics of an icefish reveals mechanisms of glacier-driven adaptive radiation in Antarctic notothenioids |
| title_full | Population genomics of an icefish reveals mechanisms of glacier-driven adaptive radiation in Antarctic notothenioids |
| title_fullStr | Population genomics of an icefish reveals mechanisms of glacier-driven adaptive radiation in Antarctic notothenioids |
| title_full_unstemmed | Population genomics of an icefish reveals mechanisms of glacier-driven adaptive radiation in Antarctic notothenioids |
| title_short | Population genomics of an icefish reveals mechanisms of glacier-driven adaptive radiation in Antarctic notothenioids |
| title_sort | population genomics of an icefish reveals mechanisms of glacier driven adaptive radiation in antarctic notothenioids |
| topic | Quaternary glacial cycles Selection sweep Reproductive isolation Gut microbiota Adaptive radiation |
| url | https://doi.org/10.1186/s12915-022-01432-x |
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