Cargando…

Maintenance of quantitative genetic variance in complex, multitrait phenotypes: the contribution of rare, large effect variants in 2 Drosophila species

The interaction of evolutionary processes to determine quantitative genetic variation has implications for contemporary and future phenotypic evolution, as well as for our ability to detect causal genetic variants. While theoretical studies have provided robust predictions to discriminate among comp...

Descripción completa

Detalles Bibliográficos
Autores principales: Hine, Emma, Runcie, Daniel E, Allen, Scott L, Wang, Yiguan, Chenoweth, Stephen F, Blows, Mark W, McGuigan, Katrina
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9526065/
https://www.ncbi.nlm.nih.gov/pubmed/35961029
http://dx.doi.org/10.1093/genetics/iyac122
_version_ 1784800797038477312
author Hine, Emma
Runcie, Daniel E
Allen, Scott L
Wang, Yiguan
Chenoweth, Stephen F
Blows, Mark W
McGuigan, Katrina
author_facet Hine, Emma
Runcie, Daniel E
Allen, Scott L
Wang, Yiguan
Chenoweth, Stephen F
Blows, Mark W
McGuigan, Katrina
author_sort Hine, Emma
collection PubMed
description The interaction of evolutionary processes to determine quantitative genetic variation has implications for contemporary and future phenotypic evolution, as well as for our ability to detect causal genetic variants. While theoretical studies have provided robust predictions to discriminate among competing models, empirical assessment of these has been limited. In particular, theory highlights the importance of pleiotropy in resolving observations of selection and mutation, but empirical investigations have typically been limited to few traits. Here, we applied high-dimensional Bayesian Sparse Factor Genetic modeling to gene expression datasets in 2 species, Drosophila melanogaster and Drosophila serrata, to explore the distributions of genetic variance across high-dimensional phenotypic space. Surprisingly, most of the heritable trait covariation was due to few lines (genotypes) with extreme [>3 interquartile ranges (IQR) from the median] values. Intriguingly, while genotypes extreme for a multivariate factor also tended to have a higher proportion of individual traits that were extreme, we also observed genotypes that were extreme for multivariate factors but not for any individual trait. We observed other consistent differences between heritable multivariate factors with outlier lines vs those factors without extreme values, including differences in gene functions. We use these observations to identify further data required to advance our understanding of the evolutionary dynamics and nature of standing genetic variation for quantitative traits.
format Online
Article
Text
id pubmed-9526065
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Oxford University Press
record_format MEDLINE/PubMed
spelling pubmed-95260652022-10-03 Maintenance of quantitative genetic variance in complex, multitrait phenotypes: the contribution of rare, large effect variants in 2 Drosophila species Hine, Emma Runcie, Daniel E Allen, Scott L Wang, Yiguan Chenoweth, Stephen F Blows, Mark W McGuigan, Katrina Genetics Investigation The interaction of evolutionary processes to determine quantitative genetic variation has implications for contemporary and future phenotypic evolution, as well as for our ability to detect causal genetic variants. While theoretical studies have provided robust predictions to discriminate among competing models, empirical assessment of these has been limited. In particular, theory highlights the importance of pleiotropy in resolving observations of selection and mutation, but empirical investigations have typically been limited to few traits. Here, we applied high-dimensional Bayesian Sparse Factor Genetic modeling to gene expression datasets in 2 species, Drosophila melanogaster and Drosophila serrata, to explore the distributions of genetic variance across high-dimensional phenotypic space. Surprisingly, most of the heritable trait covariation was due to few lines (genotypes) with extreme [>3 interquartile ranges (IQR) from the median] values. Intriguingly, while genotypes extreme for a multivariate factor also tended to have a higher proportion of individual traits that were extreme, we also observed genotypes that were extreme for multivariate factors but not for any individual trait. We observed other consistent differences between heritable multivariate factors with outlier lines vs those factors without extreme values, including differences in gene functions. We use these observations to identify further data required to advance our understanding of the evolutionary dynamics and nature of standing genetic variation for quantitative traits. Oxford University Press 2022-08-12 /pmc/articles/PMC9526065/ /pubmed/35961029 http://dx.doi.org/10.1093/genetics/iyac122 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of Genetics Society of America. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Investigation
Hine, Emma
Runcie, Daniel E
Allen, Scott L
Wang, Yiguan
Chenoweth, Stephen F
Blows, Mark W
McGuigan, Katrina
Maintenance of quantitative genetic variance in complex, multitrait phenotypes: the contribution of rare, large effect variants in 2 Drosophila species
title Maintenance of quantitative genetic variance in complex, multitrait phenotypes: the contribution of rare, large effect variants in 2 Drosophila species
title_full Maintenance of quantitative genetic variance in complex, multitrait phenotypes: the contribution of rare, large effect variants in 2 Drosophila species
title_fullStr Maintenance of quantitative genetic variance in complex, multitrait phenotypes: the contribution of rare, large effect variants in 2 Drosophila species
title_full_unstemmed Maintenance of quantitative genetic variance in complex, multitrait phenotypes: the contribution of rare, large effect variants in 2 Drosophila species
title_short Maintenance of quantitative genetic variance in complex, multitrait phenotypes: the contribution of rare, large effect variants in 2 Drosophila species
title_sort maintenance of quantitative genetic variance in complex, multitrait phenotypes: the contribution of rare, large effect variants in 2 drosophila species
topic Investigation
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9526065/
https://www.ncbi.nlm.nih.gov/pubmed/35961029
http://dx.doi.org/10.1093/genetics/iyac122
work_keys_str_mv AT hineemma maintenanceofquantitativegeneticvarianceincomplexmultitraitphenotypesthecontributionofrarelargeeffectvariantsin2drosophilaspecies
AT runciedaniele maintenanceofquantitativegeneticvarianceincomplexmultitraitphenotypesthecontributionofrarelargeeffectvariantsin2drosophilaspecies
AT allenscottl maintenanceofquantitativegeneticvarianceincomplexmultitraitphenotypesthecontributionofrarelargeeffectvariantsin2drosophilaspecies
AT wangyiguan maintenanceofquantitativegeneticvarianceincomplexmultitraitphenotypesthecontributionofrarelargeeffectvariantsin2drosophilaspecies
AT chenowethstephenf maintenanceofquantitativegeneticvarianceincomplexmultitraitphenotypesthecontributionofrarelargeeffectvariantsin2drosophilaspecies
AT blowsmarkw maintenanceofquantitativegeneticvarianceincomplexmultitraitphenotypesthecontributionofrarelargeeffectvariantsin2drosophilaspecies
AT mcguigankatrina maintenanceofquantitativegeneticvarianceincomplexmultitraitphenotypesthecontributionofrarelargeeffectvariantsin2drosophilaspecies