Mapping epigenetic divergence in the massive radiation of Lake Malawi cichlid fishes

Grégoire Vernaz; Milan Malinsky; Hannes Svardal; Mingliu Du; Alexandra M. Tyers; M. Emília Santos; Richard Durbin; Martin J. Genner; George F. Turner; Eric A. Miska

doi:10.1038/s41467-021-26166-2

Mapping epigenetic divergence in the massive radiation of Lake Malawi cichlid fishes

Grégoire Vernaz^*
, Milan Malinsky
, Hannes Svardal
, Mingliu Du
, Alexandra M. Tyers
, M. Emília Santos
, Richard Durbin
, Martin J. Genner
, George F. Turner
, Eric A. Miska

^*Corresponding author for this work

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Abstract

Epigenetic variation modulates gene expression and can be heritable. However, knowledge of the contribution of epigenetic divergence to adaptive diversification in nature remains limited. The massive evolutionary radiation of Lake Malawi cichlid fishes displaying extensive phenotypic diversity despite extremely low sequence divergence is an excellent system to study the epigenomic contribution to adaptation. Here, we present a comparative genome-wide methylome and transcriptome study, focussing on liver and muscle tissues in phenotypically divergent cichlid species. In both tissues we find substantial methylome divergence among species. Differentially methylated regions (DMR), enriched in evolutionary young transposons, are associated with transcription changes of ecologically-relevant genes related to energy expenditure and lipid metabolism, pointing to a link between dietary ecology and methylome divergence. Unexpectedly, half of all species-specific DMRs are shared across tissues and are enriched in developmental genes, likely reflecting distinct epigenetic developmental programmes. Our study reveals substantial methylome divergence in closely-related cichlid fishes and represents a resource to study the role of epigenetics in species diversification.

Original language	English
Article number	5870
Journal	Nature Communications
Volume	12
Issue number	1
DOIs	https://doi.org/10.1038/s41467-021-26166-2
Publication status	Published - 7 Oct 2021

Bibliographical note

Funding Information:
We would like to thank S.M. Grant’s diving team for collecting some of the fish specimens, as well as the Fisheries Research Unit of the Government of Malawi, and the Tanzania Fisheries Research Institute, for their assistance and support. We would like to thank the staff at the Gurdon Institute and the sequencing facilities at CRUK Cambridge Institute, Gurdon, and Sanger Institutes for their expertise and support. We would like to thank the members of the Miska Lab as well as the Cambridge Cichlid community for fruitful discussions. We thank Navin B. Ramakrishna for critical comments on the manuscript, as well as David Jordan, Tomás di Domenico and Konrad L.M. Rudolph for their support with data analysis. We are grateful to Ole Seehausen and Marcel Häsler (University of Bern, Switzerland) for providing PN tissues. We thank Alan Hudson for help with sample collection. The map of Africa (Fig. 1a) was downloaded and modified from https://www.d-maps.com/carte.php?num_car=733&lang=en. This work was supported by the following grants to E.A.M.: Wellcome Trust Senior Investigator Award (104640/Z/14/Z and 219475/Z/19/Z) and CRUK award (C13474/A27826); to R.D.: Wellcome award (WT207492); to G.F.T. and M.J.G., the Leverhulme Trust—Royal Society Africa Awards (AA100023 and AA130107), and NERC award (NE/S001794/1). G.V. thanks Wolfson College, University of Cambridge, and the Genetics Society, London for financial support. The authors also acknowledge core funding to the Gurdon Institute from Wellcome (092096/Z/10/Z, 203144/Z/16/Z) and CRUK (C6946/A24843). For Open Access, the author has applied a CC BY public copyright licence to any Author Accepted Manuscript version arising from this submission.

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© 2021, Crown.

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@article{f19af8fca90a4d678b72fd452afaed23,

title = "Mapping epigenetic divergence in the massive radiation of Lake Malawi cichlid fishes",

abstract = "Epigenetic variation modulates gene expression and can be heritable. However, knowledge of the contribution of epigenetic divergence to adaptive diversification in nature remains limited. The massive evolutionary radiation of Lake Malawi cichlid fishes displaying extensive phenotypic diversity despite extremely low sequence divergence is an excellent system to study the epigenomic contribution to adaptation. Here, we present a comparative genome-wide methylome and transcriptome study, focussing on liver and muscle tissues in phenotypically divergent cichlid species. In both tissues we find substantial methylome divergence among species. Differentially methylated regions (DMR), enriched in evolutionary young transposons, are associated with transcription changes of ecologically-relevant genes related to energy expenditure and lipid metabolism, pointing to a link between dietary ecology and methylome divergence. Unexpectedly, half of all species-specific DMRs are shared across tissues and are enriched in developmental genes, likely reflecting distinct epigenetic developmental programmes. Our study reveals substantial methylome divergence in closely-related cichlid fishes and represents a resource to study the role of epigenetics in species diversification.",

author = "Gr{\'e}goire Vernaz and Milan Malinsky and Hannes Svardal and Mingliu Du and Tyers, \{Alexandra M.\} and Santos, \{M. Em{\'i}lia\} and Richard Durbin and Genner, \{Martin J.\} and Turner, \{George F.\} and Miska, \{Eric A.\}",

note = "Funding Information: We would like to thank S.M. Grant{\textquoteright}s diving team for collecting some of the fish specimens, as well as the Fisheries Research Unit of the Government of Malawi, and the Tanzania Fisheries Research Institute, for their assistance and support. We would like to thank the staff at the Gurdon Institute and the sequencing facilities at CRUK Cambridge Institute, Gurdon, and Sanger Institutes for their expertise and support. We would like to thank the members of the Miska Lab as well as the Cambridge Cichlid community for fruitful discussions. We thank Navin B. Ramakrishna for critical comments on the manuscript, as well as David Jordan, Tom{\'a}s di Domenico and Konrad L.M. Rudolph for their support with data analysis. We are grateful to Ole Seehausen and Marcel H{\"a}sler (University of Bern, Switzerland) for providing PN tissues. We thank Alan Hudson for help with sample collection. The map of Africa (Fig. 1a) was downloaded and modified from https://www.d-maps.com/carte.php?num\_car=733\&lang=en. This work was supported by the following grants to E.A.M.: Wellcome Trust Senior Investigator Award (104640/Z/14/Z and 219475/Z/19/Z) and CRUK award (C13474/A27826); to R.D.: Wellcome award (WT207492); to G.F.T. and M.J.G., the Leverhulme Trust—Royal Society Africa Awards (AA100023 and AA130107), and NERC award (NE/S001794/1). G.V. thanks Wolfson College, University of Cambridge, and the Genetics Society, London for financial support. The authors also acknowledge core funding to the Gurdon Institute from Wellcome (092096/Z/10/Z, 203144/Z/16/Z) and CRUK (C6946/A24843). For Open Access, the author has applied a CC BY public copyright licence to any Author Accepted Manuscript version arising from this submission. Publisher Copyright: {\textcopyright} 2021, Crown.",

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doi = "10.1038/s41467-021-26166-2",

language = "English",

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T1 - Mapping epigenetic divergence in the massive radiation of Lake Malawi cichlid fishes

AU - Vernaz, Grégoire

AU - Malinsky, Milan

AU - Svardal, Hannes

AU - Du, Mingliu

AU - Tyers, Alexandra M.

AU - Santos, M. Emília

AU - Durbin, Richard

AU - Genner, Martin J.

AU - Turner, George F.

AU - Miska, Eric A.

N1 - Funding Information: We would like to thank S.M. Grant’s diving team for collecting some of the fish specimens, as well as the Fisheries Research Unit of the Government of Malawi, and the Tanzania Fisheries Research Institute, for their assistance and support. We would like to thank the staff at the Gurdon Institute and the sequencing facilities at CRUK Cambridge Institute, Gurdon, and Sanger Institutes for their expertise and support. We would like to thank the members of the Miska Lab as well as the Cambridge Cichlid community for fruitful discussions. We thank Navin B. Ramakrishna for critical comments on the manuscript, as well as David Jordan, Tomás di Domenico and Konrad L.M. Rudolph for their support with data analysis. We are grateful to Ole Seehausen and Marcel Häsler (University of Bern, Switzerland) for providing PN tissues. We thank Alan Hudson for help with sample collection. The map of Africa (Fig. 1a) was downloaded and modified from https://www.d-maps.com/carte.php?num_car=733&lang=en. This work was supported by the following grants to E.A.M.: Wellcome Trust Senior Investigator Award (104640/Z/14/Z and 219475/Z/19/Z) and CRUK award (C13474/A27826); to R.D.: Wellcome award (WT207492); to G.F.T. and M.J.G., the Leverhulme Trust—Royal Society Africa Awards (AA100023 and AA130107), and NERC award (NE/S001794/1). G.V. thanks Wolfson College, University of Cambridge, and the Genetics Society, London for financial support. The authors also acknowledge core funding to the Gurdon Institute from Wellcome (092096/Z/10/Z, 203144/Z/16/Z) and CRUK (C6946/A24843). For Open Access, the author has applied a CC BY public copyright licence to any Author Accepted Manuscript version arising from this submission. Publisher Copyright: © 2021, Crown.

PY - 2021/10/7

Y1 - 2021/10/7

N2 - Epigenetic variation modulates gene expression and can be heritable. However, knowledge of the contribution of epigenetic divergence to adaptive diversification in nature remains limited. The massive evolutionary radiation of Lake Malawi cichlid fishes displaying extensive phenotypic diversity despite extremely low sequence divergence is an excellent system to study the epigenomic contribution to adaptation. Here, we present a comparative genome-wide methylome and transcriptome study, focussing on liver and muscle tissues in phenotypically divergent cichlid species. In both tissues we find substantial methylome divergence among species. Differentially methylated regions (DMR), enriched in evolutionary young transposons, are associated with transcription changes of ecologically-relevant genes related to energy expenditure and lipid metabolism, pointing to a link between dietary ecology and methylome divergence. Unexpectedly, half of all species-specific DMRs are shared across tissues and are enriched in developmental genes, likely reflecting distinct epigenetic developmental programmes. Our study reveals substantial methylome divergence in closely-related cichlid fishes and represents a resource to study the role of epigenetics in species diversification.

AB - Epigenetic variation modulates gene expression and can be heritable. However, knowledge of the contribution of epigenetic divergence to adaptive diversification in nature remains limited. The massive evolutionary radiation of Lake Malawi cichlid fishes displaying extensive phenotypic diversity despite extremely low sequence divergence is an excellent system to study the epigenomic contribution to adaptation. Here, we present a comparative genome-wide methylome and transcriptome study, focussing on liver and muscle tissues in phenotypically divergent cichlid species. In both tissues we find substantial methylome divergence among species. Differentially methylated regions (DMR), enriched in evolutionary young transposons, are associated with transcription changes of ecologically-relevant genes related to energy expenditure and lipid metabolism, pointing to a link between dietary ecology and methylome divergence. Unexpectedly, half of all species-specific DMRs are shared across tissues and are enriched in developmental genes, likely reflecting distinct epigenetic developmental programmes. Our study reveals substantial methylome divergence in closely-related cichlid fishes and represents a resource to study the role of epigenetics in species diversification.

UR - https://www.scopus.com/pages/publications/85116595431

U2 - 10.1038/s41467-021-26166-2

DO - 10.1038/s41467-021-26166-2

M3 - Article (Academic Journal)

C2 - 34620871

AN - SCOPUS:85116595431

SN - 2041-1723

VL - 12

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 5870

ER -

Mapping epigenetic divergence in the massive radiation of Lake Malawi cichlid fishes

Abstract

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Characterising the biodiversity of freshwater fishes of Africa using environmental DNA metabarcoding: A case study within the Kilombero river system of Tanzania

Can phenotypic plasticity and DNA methylation promote adaptive radiation?

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Mapping epigenetic divergence in the massive radiation of Lake Malawi cichlid fishes

Abstract

Bibliographical note

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Characterising the biodiversity of freshwater fishes of Africa using environmental DNA metabarcoding: A case study within the Kilombero river system of Tanzania

Can phenotypic plasticity and DNA methylation promote adaptive radiation?

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