Extensive standing genetic variation from a small number of founders enables rapid adaptation in Daphnia

Anurag Chaturvedi; Jiarui Zhou; Joost A. M. Raeymaekers; Luisa Orsini; Till  Czypionka; Craig E. Jackson; Katina I Spanier; Joseph R Shaw; John Colbourne; Luc De Meester

doi:10.1038/s41467-021-24581-z

Extensive standing genetic variation from a small number of founders enables rapid adaptation in Daphnia

Anurag Chaturvedi, Jiarui Zhou, Joost A. M. Raeymaekers, Luisa Orsini, Till Czypionka, Craig E. Jackson, Katina I Spanier, Joseph R Shaw, John Colbourne, Luc De Meester

Biosciences

Research output: Contribution to journal › Article › peer-review

124 Downloads (Pure)

Abstract

We lack a thorough understanding of the origin and maintenance of standing genetic variation that enables rapid evolutionary responses of natural populations. Whole genome sequencing of a resurrected Daphnia population shows that standing genetic variation in over 500 genes follows an evolutionary trajectory that parallels the pronounced and rapid adaptive evolution of multiple traits in response to predator-driven natural selection and its subsequent relaxation. Genetic variation carried by only five founding individuals from the regional genotype pool is shown to suffice at enabling the observed evolution. Our results provide insight on how natural populations can acquire the genomic variation, through colonization by a few regional genotypes, that fuels rapid evolution in response to strong selection pressures. While these evolutionary responses in our study population involved hundreds of genes, we observed no evidence of genetic erosion.

Original language	English
Article number	4306
Number of pages	1
Journal	Nature Communications
Volume	12
Issue number	1
DOIs	https://doi.org/10.1038/s41467-021-24581-z
Publication status	Published - 14 Jul 2021

Bibliographical note

Funding Information:
We gratefully acknowledge financial support from KU Leuven Research Fund projects PF/2010/07 and C16/2017/002, from FWO projects G.0468.10, G.0614.11, G0B9818, and G0C3818, and from NERC project NE/N016777/1. KIS was supported by a PhD fellowship of the Agency for Innovation by Science and Technology in Flanders (IWT) and TC was supported by a DFG Research Fellowship (CZ 230 1/1). We thank Edson Sandoval-Castellanos for providing source code of the TAFT software and the Daphnia Genomics Consortium, including Don Gilbert (Indiana University) for its collective efforts to assemble and annotate the D. magna genome.

Publisher Copyright:
© 2021, The Author(s).

Keywords

Adaptation, Physiological/genetics
Animals
Biological Evolution
Daphnia/genetics
Founder Effect
Gene Frequency
Genetic Variation
Genetics, Population
Genome/genetics
Genotype
Phenotype
Selection, Genetic

Access to Document

10.1038/s41467-021-24581-zLicence: Creative Commons: Attribution (CC BY)

ChaturvediA2021ExtensiveFinal published version, 1.53 MBLicence: Creative Commons: Attribution (CC BY)

Cracking the Code of Adaptive Evolution (deCODE)
Brown, J., Orsini, L., Viant, M., Compton, L., Colbourne, J., He, S. & Windridge, D.
Natural Environment Research Council
1/05/16 → 31/01/22
Project: Research Councils

Cite this

@article{31b441f45acd4556bd12373bfe425f22,

title = "Extensive standing genetic variation from a small number of founders enables rapid adaptation in Daphnia",

abstract = "We lack a thorough understanding of the origin and maintenance of standing genetic variation that enables rapid evolutionary responses of natural populations. Whole genome sequencing of a resurrected Daphnia population shows that standing genetic variation in over 500 genes follows an evolutionary trajectory that parallels the pronounced and rapid adaptive evolution of multiple traits in response to predator-driven natural selection and its subsequent relaxation. Genetic variation carried by only five founding individuals from the regional genotype pool is shown to suffice at enabling the observed evolution. Our results provide insight on how natural populations can acquire the genomic variation, through colonization by a few regional genotypes, that fuels rapid evolution in response to strong selection pressures. While these evolutionary responses in our study population involved hundreds of genes, we observed no evidence of genetic erosion.",

keywords = "Adaptation, Physiological/genetics, Animals, Biological Evolution, Daphnia/genetics, Founder Effect, Gene Frequency, Genetic Variation, Genetics, Population, Genome/genetics, Genotype, Phenotype, Selection, Genetic",

author = "Anurag Chaturvedi and Jiarui Zhou and Raeymaekers, {Joost A. M.} and Luisa Orsini and Till Czypionka and Jackson, {Craig E.} and Spanier, {Katina I} and Shaw, {Joseph R} and John Colbourne and {De Meester}, Luc",

note = "Funding Information: We gratefully acknowledge financial support from KU Leuven Research Fund projects PF/2010/07 and C16/2017/002, from FWO projects G.0468.10, G.0614.11, G0B9818, and G0C3818, and from NERC project NE/N016777/1. KIS was supported by a PhD fellowship of the Agency for Innovation by Science and Technology in Flanders (IWT) and TC was supported by a DFG Research Fellowship (CZ 230 1/1). We thank Edson Sandoval-Castellanos for providing source code of the TAFT software and the Daphnia Genomics Consortium, including Don Gilbert (Indiana University) for its collective efforts to assemble and annotate the D. magna genome. Publisher Copyright: {\textcopyright} 2021, The Author(s).",

year = "2021",

month = jul,

day = "14",

doi = "10.1038/s41467-021-24581-z",

language = "English",

volume = "12",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Springer",

number = "1",

}

TY - JOUR

T1 - Extensive standing genetic variation from a small number of founders enables rapid adaptation in Daphnia

AU - Chaturvedi, Anurag

AU - Zhou, Jiarui

AU - Raeymaekers, Joost A. M.

AU - Orsini, Luisa

AU - Czypionka, Till

AU - Jackson, Craig E.

AU - Spanier, Katina I

AU - Shaw, Joseph R

AU - Colbourne, John

AU - De Meester, Luc

N1 - Funding Information: We gratefully acknowledge financial support from KU Leuven Research Fund projects PF/2010/07 and C16/2017/002, from FWO projects G.0468.10, G.0614.11, G0B9818, and G0C3818, and from NERC project NE/N016777/1. KIS was supported by a PhD fellowship of the Agency for Innovation by Science and Technology in Flanders (IWT) and TC was supported by a DFG Research Fellowship (CZ 230 1/1). We thank Edson Sandoval-Castellanos for providing source code of the TAFT software and the Daphnia Genomics Consortium, including Don Gilbert (Indiana University) for its collective efforts to assemble and annotate the D. magna genome. Publisher Copyright: © 2021, The Author(s).

PY - 2021/7/14

Y1 - 2021/7/14

N2 - We lack a thorough understanding of the origin and maintenance of standing genetic variation that enables rapid evolutionary responses of natural populations. Whole genome sequencing of a resurrected Daphnia population shows that standing genetic variation in over 500 genes follows an evolutionary trajectory that parallels the pronounced and rapid adaptive evolution of multiple traits in response to predator-driven natural selection and its subsequent relaxation. Genetic variation carried by only five founding individuals from the regional genotype pool is shown to suffice at enabling the observed evolution. Our results provide insight on how natural populations can acquire the genomic variation, through colonization by a few regional genotypes, that fuels rapid evolution in response to strong selection pressures. While these evolutionary responses in our study population involved hundreds of genes, we observed no evidence of genetic erosion.

AB - We lack a thorough understanding of the origin and maintenance of standing genetic variation that enables rapid evolutionary responses of natural populations. Whole genome sequencing of a resurrected Daphnia population shows that standing genetic variation in over 500 genes follows an evolutionary trajectory that parallels the pronounced and rapid adaptive evolution of multiple traits in response to predator-driven natural selection and its subsequent relaxation. Genetic variation carried by only five founding individuals from the regional genotype pool is shown to suffice at enabling the observed evolution. Our results provide insight on how natural populations can acquire the genomic variation, through colonization by a few regional genotypes, that fuels rapid evolution in response to strong selection pressures. While these evolutionary responses in our study population involved hundreds of genes, we observed no evidence of genetic erosion.

KW - Adaptation, Physiological/genetics

KW - Animals

KW - Biological Evolution

KW - Daphnia/genetics

KW - Founder Effect

KW - Gene Frequency

KW - Genetic Variation

KW - Genetics, Population

KW - Genome/genetics

KW - Genotype

KW - Phenotype

KW - Selection, Genetic

UR - http://www.scopus.com/inward/record.url?scp=85110619225&partnerID=8YFLogxK

U2 - 10.1038/s41467-021-24581-z

DO - 10.1038/s41467-021-24581-z

M3 - Article

C2 - 34262034

SN - 2041-1723

VL - 12

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 4306

ER -

Extensive standing genetic variation from a small number of founders enables rapid adaptation in Daphnia

Abstract

Bibliographical note

Keywords

Access to Document

Fingerprint

Projects

Cracking the Code of Adaptive Evolution (deCODE)

Cite this