Genome-wide detection of positive and balancing signatures of selection shared by four domesticated rainbow trout populations (Oncorhynchus mykiss)

Abstract Background Evolutionary processes leave footprints along the genome over time. Highly homozygous regions may correspond to positive selection of favorable alleles, while maintenance of heterozygous regions may be due to balancing selection phenomena. We analyzed data from 176 fish from four...

Full description

Bibliographic Details
Main Authors: Katy Paul, Gwendal Restoux, Florence Phocas
Format: Article
Language:deu
Published: BMC 2024-02-01
Series:Genetics Selection Evolution
Online Access:https://doi.org/10.1186/s12711-024-00884-9
_version_ 1797276192497205248
author Katy Paul
Gwendal Restoux
Florence Phocas
author_facet Katy Paul
Gwendal Restoux
Florence Phocas
author_sort Katy Paul
collection DOAJ
description Abstract Background Evolutionary processes leave footprints along the genome over time. Highly homozygous regions may correspond to positive selection of favorable alleles, while maintenance of heterozygous regions may be due to balancing selection phenomena. We analyzed data from 176 fish from four disconnected domestic rainbow trout populations that were genotyped using a high-density Axiom Trout genotyping 665K single nucleotide polymorphism array, including 20 from the US and 156 from three French lines. Using methods based on runs of homozygosity and extended haplotype homozygosity, we detected signatures of selection in these four populations. Results Nine genomic regions that included 253 genes were identified as being under positive selection in all four populations Most were located on chromosome 2 but also on chromosomes 12, 15, 16, and 20. In addition, four heterozygous regions that contain 29 genes that are putatively under balancing selection were also shared by the four populations. These were located on chromosomes 10, 13, and 19. Regardless of the homozygous or heterozygous nature of the regions, in each region, we detected several genes that are highly conserved among vertebrates due to their critical roles in cellular and nuclear organization, embryonic development, or immunity. We identified new candidate genes involved in rainbow trout fitness, as well as 17 genes that were previously identified to be under positive selection, 10 of which in other fishes (auts2, atp1b3, zp4, znf135, igf-1α, brd2, col9a2, mrap2, pbx1, and emilin-3). Conclusions Using material from disconnected populations of different origins allowed us to draw a genome-wide map of signatures of positive selection that are shared between these rainbow trout populations, and to identify several regions that are putatively under balancing selection. These results provide a valuable resource for future investigations of the dynamics of genetic diversity and genome evolution during domestication.
first_indexed 2024-03-07T15:23:56Z
format Article
id doaj.art-76eb39caaf4d4517a83b37f5fec2ca56
institution Directory Open Access Journal
issn 1297-9686
language deu
last_indexed 2024-03-07T15:23:56Z
publishDate 2024-02-01
publisher BMC
record_format Article
series Genetics Selection Evolution
spelling doaj.art-76eb39caaf4d4517a83b37f5fec2ca562024-03-05T17:25:03ZdeuBMCGenetics Selection Evolution1297-96862024-02-0156112010.1186/s12711-024-00884-9Genome-wide detection of positive and balancing signatures of selection shared by four domesticated rainbow trout populations (Oncorhynchus mykiss)Katy Paul0Gwendal Restoux1Florence Phocas2Université Paris-Saclay, INRAE, AgroParisTech, GABIUniversité Paris-Saclay, INRAE, AgroParisTech, GABIUniversité Paris-Saclay, INRAE, AgroParisTech, GABIAbstract Background Evolutionary processes leave footprints along the genome over time. Highly homozygous regions may correspond to positive selection of favorable alleles, while maintenance of heterozygous regions may be due to balancing selection phenomena. We analyzed data from 176 fish from four disconnected domestic rainbow trout populations that were genotyped using a high-density Axiom Trout genotyping 665K single nucleotide polymorphism array, including 20 from the US and 156 from three French lines. Using methods based on runs of homozygosity and extended haplotype homozygosity, we detected signatures of selection in these four populations. Results Nine genomic regions that included 253 genes were identified as being under positive selection in all four populations Most were located on chromosome 2 but also on chromosomes 12, 15, 16, and 20. In addition, four heterozygous regions that contain 29 genes that are putatively under balancing selection were also shared by the four populations. These were located on chromosomes 10, 13, and 19. Regardless of the homozygous or heterozygous nature of the regions, in each region, we detected several genes that are highly conserved among vertebrates due to their critical roles in cellular and nuclear organization, embryonic development, or immunity. We identified new candidate genes involved in rainbow trout fitness, as well as 17 genes that were previously identified to be under positive selection, 10 of which in other fishes (auts2, atp1b3, zp4, znf135, igf-1α, brd2, col9a2, mrap2, pbx1, and emilin-3). Conclusions Using material from disconnected populations of different origins allowed us to draw a genome-wide map of signatures of positive selection that are shared between these rainbow trout populations, and to identify several regions that are putatively under balancing selection. These results provide a valuable resource for future investigations of the dynamics of genetic diversity and genome evolution during domestication.https://doi.org/10.1186/s12711-024-00884-9
spellingShingle Katy Paul
Gwendal Restoux
Florence Phocas
Genome-wide detection of positive and balancing signatures of selection shared by four domesticated rainbow trout populations (Oncorhynchus mykiss)
Genetics Selection Evolution
title Genome-wide detection of positive and balancing signatures of selection shared by four domesticated rainbow trout populations (Oncorhynchus mykiss)
title_full Genome-wide detection of positive and balancing signatures of selection shared by four domesticated rainbow trout populations (Oncorhynchus mykiss)
title_fullStr Genome-wide detection of positive and balancing signatures of selection shared by four domesticated rainbow trout populations (Oncorhynchus mykiss)
title_full_unstemmed Genome-wide detection of positive and balancing signatures of selection shared by four domesticated rainbow trout populations (Oncorhynchus mykiss)
title_short Genome-wide detection of positive and balancing signatures of selection shared by four domesticated rainbow trout populations (Oncorhynchus mykiss)
title_sort genome wide detection of positive and balancing signatures of selection shared by four domesticated rainbow trout populations oncorhynchus mykiss
url https://doi.org/10.1186/s12711-024-00884-9
work_keys_str_mv AT katypaul genomewidedetectionofpositiveandbalancingsignaturesofselectionsharedbyfourdomesticatedrainbowtroutpopulationsoncorhynchusmykiss
AT gwendalrestoux genomewidedetectionofpositiveandbalancingsignaturesofselectionsharedbyfourdomesticatedrainbowtroutpopulationsoncorhynchusmykiss
AT florencephocas genomewidedetectionofpositiveandbalancingsignaturesofselectionsharedbyfourdomesticatedrainbowtroutpopulationsoncorhynchusmykiss