Epigenetic divergence during early stages of speciation in an African crater lake cichlid fish

Grégoire Vernaz; Alan G Hudson; M Emília Santos; Bettina Fischer; Madeleine Carruthers; Asilatu H Shechonge; Nestory P Gabagambi; Alexandra M Tyers; Benjamin P Ngatunga; Milan Malinsky; Richard Durbin; George F Turner; Martin J Genner; Eric A Miska

doi:10.1038/s41559-022-01894-w

Epigenetic divergence during early stages of speciation in an African crater lake cichlid fish

Grégoire Vernaz^*
, Alan G Hudson
, M Emília Santos
, Bettina Fischer
, Madeleine Carruthers
, Asilatu H Shechonge
, Nestory P Gabagambi
, Alexandra M Tyers
, Benjamin P Ngatunga
, Milan Malinsky
, Richard Durbin
, George F Turner
, Martin J Genner^*
, Eric A Miska^*

^*Corresponding author for this work

Research output: Contribution to journal › Article (Academic Journal) › peer-review

38 Citations (Scopus)

80 Downloads (Pure)

Abstract

Epigenetic variation can alter transcription and promote phenotypic divergence between populations facing different environmental challenges. Here, we assess the epigenetic basis of diversification during the early stages of speciation. Specifically, we focus on the extent and functional relevance of DNA methylome divergence in the very young radiation of Astatotilapia calliptera in crater Lake Masoko, southern Tanzania. Our study focuses on two lake ecomorphs that diverged approximately 1,000 years ago and a population in the nearby river from which they separated approximately 10,000 years ago. The two lake ecomorphs show no fixed genetic differentiation, yet are characterized by different morphologies, depth preferences and diets. We report extensive genome-wide methylome divergence between the two lake ecomorphs, and between the lake and river populations, linked to key biological processes and associated with altered transcriptional activity of ecologically relevant genes. Such genes differing between lake ecomorphs include those involved in steroid metabolism, hemoglobin composition and erythropoiesis, consistent with their divergent habitat occupancy. Using a common-garden experiment, we found that global methylation profiles are often rapidly remodeled across generations but ecomorph-specific differences can be inherited. Collectively, our study suggests an epigenetic contribution to the early stages of vertebrate speciation.

Original language	English
Pages (from-to)	1940-1951
Number of pages	12
Journal	Nature Ecology and Evolution
Volume	6
Issue number	12
Early online date	20 Oct 2022
DOIs	https://doi.org/10.1038/s41559-022-01894-w
Publication status	E-pub ahead of print - 20 Oct 2022

Bibliographical note

Funding Information:
We thank the staff of the Tanzania Fisheries Research Institute for their assistance and support. The Tanzania Commission for Science and Technology provided research permits and the Tanzania Ministry of Livestock and Fisheries provided export permits. We thank M. Ndawala (TAFIRI) and G. Kazumbe for their help with sample collection, and J. Johnson for her fish paintings. We thank N. B. Ramakrishna for critical comments on the manuscript, the staff at the Gurdon Institute and the sequencing facilities at the Cancer Research UK (CRUK) Cambridge Institute, Wellcome Gurdon and Wellcome Sanger Institutes, and Genomics facility at the University of Bristol for their expertise and support. This work was supported by the following grants to E.A.M.: Wellcome Trust Senior Investigator award (nos. 104640/Z/14/Z and 219475/Z/19/Z) and CRUK award (no. C13474/A27826); to R.D.: Wellcome award (no. WT207492); to G.F.T.: Leverhulme Trust Award no. RPG-2014-214; to M.J.G., G.F.T. and B.P.N.: the Leverhulme Trust – Royal Society Africa Awards (nos. AA100023 and AA130107); to M.J.G. and G.F.T.: Natural Environment Research Council (NERC) award (no. NE/S001794/1); to M.J.G.: Leverhulme Trust award (no. RF-2014-686); to A.G.H.: Marie Skłodowska-Curie Individual Fellowship (no. GA-659791). G.V. acknowledges Wolfson College, University of Cambridge, and the Genetics Society, London, for financial support. M.E.S. is supported by an NERC Independent Research Fellowship no. NE/R01504X/1. The authors also acknowledge core funding to the Gurdon Institute from Wellcome (nos. 092096/Z/10/Z, 203144/Z/16/Z) and CRUK (no. C6946/A24843). For open access, the authors have applied a CC BY public copyright licence to any author-accepted manuscript version arising from this submission.

Funding Information:
We thank the staff of the Tanzania Fisheries Research Institute for their assistance and support. The Tanzania Commission for Science and Technology provided research permits and the Tanzania Ministry of Livestock and Fisheries provided export permits. We thank M. Ndawala (TAFIRI) and G. Kazumbe for their help with sample collection, and J. Johnson for her fish paintings. We thank N. B. Ramakrishna for critical comments on the manuscript, the staff at the Gurdon Institute and the sequencing facilities at the Cancer Research UK (CRUK) Cambridge Institute, Wellcome Gurdon and Wellcome Sanger Institutes, and Genomics facility at the University of Bristol for their expertise and support. This work was supported by the following grants to E.A.M.: Wellcome Trust Senior Investigator award (nos. 104640/Z/14/Z and 219475/Z/19/Z) and CRUK award (no. C13474/A27826); to R.D.: Wellcome award (no. WT207492); to G.F.T.: Leverhulme Trust Award no. RPG-2014-214; to M.J.G., G.F.T. and B.P.N.: the Leverhulme Trust – Royal Society Africa Awards (nos. AA100023 and AA130107); to M.J.G. and G.F.T.: Natural Environment Research Council (NERC) award (no. NE/S001794/1); to M.J.G.: Leverhulme Trust award (no. RF-2014-686); to A.G.H.: Marie Skłodowska-Curie Individual Fellowship (no. GA-659791). G.V. acknowledges Wolfson College, University of Cambridge, and the Genetics Society, London, for financial support. M.E.S. is supported by an NERC Independent Research Fellowship no. NE/R01504X/1. The authors also acknowledge core funding to the Gurdon Institute from Wellcome (nos. 092096/Z/10/Z, 203144/Z/16/Z) and CRUK (no. C6946/A24843). For open access, the authors have applied a CC BY public copyright licence to any author-accepted manuscript version arising from this submission.

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Vernaz, G., Hudson, A. G., Santos, M. E., Fischer, B., Carruthers, M., Shechonge, A. H., Gabagambi, N. P., Tyers, A. M., Ngatunga, B. P., Malinsky, M., Durbin, R., Turner, G. F., Genner, M. J., & Miska, E. A. (2022). Epigenetic divergence during early stages of speciation in an African crater lake cichlid fish. Nature Ecology and Evolution, 6(12), 1940-1951. Advance online publication. https://doi.org/10.1038/s41559-022-01894-w

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abstract = "Epigenetic variation can alter transcription and promote phenotypic divergence between populations facing different environmental challenges. Here, we assess the epigenetic basis of diversification during the early stages of speciation. Specifically, we focus on the extent and functional relevance of DNA methylome divergence in the very young radiation of Astatotilapia calliptera in crater Lake Masoko, southern Tanzania. Our study focuses on two lake ecomorphs that diverged approximately 1,000 years ago and a population in the nearby river from which they separated approximately 10,000 years ago. The two lake ecomorphs show no fixed genetic differentiation, yet are characterized by different morphologies, depth preferences and diets. We report extensive genome-wide methylome divergence between the two lake ecomorphs, and between the lake and river populations, linked to key biological processes and associated with altered transcriptional activity of ecologically relevant genes. Such genes differing between lake ecomorphs include those involved in steroid metabolism, hemoglobin composition and erythropoiesis, consistent with their divergent habitat occupancy. Using a common-garden experiment, we found that global methylation profiles are often rapidly remodeled across generations but ecomorph-specific differences can be inherited. Collectively, our study suggests an epigenetic contribution to the early stages of vertebrate speciation.",

author = "Gr{\'e}goire Vernaz and Hudson, \{Alan G\} and Santos, \{M Em{\'i}lia\} and Bettina Fischer and Madeleine Carruthers and Shechonge, \{Asilatu H\} and Gabagambi, \{Nestory P\} and Tyers, \{Alexandra M\} and Ngatunga, \{Benjamin P\} and Milan Malinsky and Richard Durbin and Turner, \{George F\} and Genner, \{Martin J\} and Miska, \{Eric A\}",

note = "Funding Information: We thank the staff of the Tanzania Fisheries Research Institute for their assistance and support. The Tanzania Commission for Science and Technology provided research permits and the Tanzania Ministry of Livestock and Fisheries provided export permits. We thank M. Ndawala (TAFIRI) and G. Kazumbe for their help with sample collection, and J. Johnson for her fish paintings. We thank N. B. Ramakrishna for critical comments on the manuscript, the staff at the Gurdon Institute and the sequencing facilities at the Cancer Research UK (CRUK) Cambridge Institute, Wellcome Gurdon and Wellcome Sanger Institutes, and Genomics facility at the University of Bristol for their expertise and support. This work was supported by the following grants to E.A.M.: Wellcome Trust Senior Investigator award (nos. 104640/Z/14/Z and 219475/Z/19/Z) and CRUK award (no. C13474/A27826); to R.D.: Wellcome award (no. WT207492); to G.F.T.: Leverhulme Trust Award no. RPG-2014-214; to M.J.G., G.F.T. and B.P.N.: the Leverhulme Trust {\textendash} Royal Society Africa Awards (nos. AA100023 and AA130107); to M.J.G. and G.F.T.: Natural Environment Research Council (NERC) award (no. NE/S001794/1); to M.J.G.: Leverhulme Trust award (no. RF-2014-686); to A.G.H.: Marie Sk{\l}odowska-Curie Individual Fellowship (no. GA-659791). G.V. acknowledges Wolfson College, University of Cambridge, and the Genetics Society, London, for financial support. M.E.S. is supported by an NERC Independent Research Fellowship no. NE/R01504X/1. The authors also acknowledge core funding to the Gurdon Institute from Wellcome (nos. 092096/Z/10/Z, 203144/Z/16/Z) and CRUK (no. C6946/A24843). For open access, the authors have applied a CC BY public copyright licence to any author-accepted manuscript version arising from this submission. Funding Information: We thank the staff of the Tanzania Fisheries Research Institute for their assistance and support. The Tanzania Commission for Science and Technology provided research permits and the Tanzania Ministry of Livestock and Fisheries provided export permits. We thank M. Ndawala (TAFIRI) and G. Kazumbe for their help with sample collection, and J. Johnson for her fish paintings. We thank N. B. Ramakrishna for critical comments on the manuscript, the staff at the Gurdon Institute and the sequencing facilities at the Cancer Research UK (CRUK) Cambridge Institute, Wellcome Gurdon and Wellcome Sanger Institutes, and Genomics facility at the University of Bristol for their expertise and support. This work was supported by the following grants to E.A.M.: Wellcome Trust Senior Investigator award (nos. 104640/Z/14/Z and 219475/Z/19/Z) and CRUK award (no. C13474/A27826); to R.D.: Wellcome award (no. WT207492); to G.F.T.: Leverhulme Trust Award no. RPG-2014-214; to M.J.G., G.F.T. and B.P.N.: the Leverhulme Trust {\textendash} Royal Society Africa Awards (nos. AA100023 and AA130107); to M.J.G. and G.F.T.: Natural Environment Research Council (NERC) award (no. NE/S001794/1); to M.J.G.: Leverhulme Trust award (no. RF-2014-686); to A.G.H.: Marie Sk{\l}odowska-Curie Individual Fellowship (no. GA-659791). G.V. acknowledges Wolfson College, University of Cambridge, and the Genetics Society, London, for financial support. M.E.S. is supported by an NERC Independent Research Fellowship no. NE/R01504X/1. The authors also acknowledge core funding to the Gurdon Institute from Wellcome (nos. 092096/Z/10/Z, 203144/Z/16/Z) and CRUK (no. C6946/A24843). For open access, the authors have applied a CC BY public copyright licence to any author-accepted manuscript version arising from this submission. Publisher Copyright: {\textcopyright} 2022, The Author(s).",

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Vernaz, G, Hudson, AG, Santos, ME, Fischer, B, Carruthers, M, Shechonge, AH, Gabagambi, NP, Tyers, AM, Ngatunga, BP, Malinsky, M, Durbin, R, Turner, GF, Genner, MJ & Miska, EA 2022, 'Epigenetic divergence during early stages of speciation in an African crater lake cichlid fish', Nature Ecology and Evolution, vol. 6, no. 12, pp. 1940-1951. https://doi.org/10.1038/s41559-022-01894-w

TY - JOUR

T1 - Epigenetic divergence during early stages of speciation in an African crater lake cichlid fish

AU - Vernaz, Grégoire

AU - Hudson, Alan G

AU - Santos, M Emília

AU - Fischer, Bettina

AU - Carruthers, Madeleine

AU - Shechonge, Asilatu H

AU - Gabagambi, Nestory P

AU - Tyers, Alexandra M

AU - Ngatunga, Benjamin P

AU - Malinsky, Milan

AU - Durbin, Richard

AU - Turner, George F

AU - Genner, Martin J

AU - Miska, Eric A

N1 - Funding Information: We thank the staff of the Tanzania Fisheries Research Institute for their assistance and support. The Tanzania Commission for Science and Technology provided research permits and the Tanzania Ministry of Livestock and Fisheries provided export permits. We thank M. Ndawala (TAFIRI) and G. Kazumbe for their help with sample collection, and J. Johnson for her fish paintings. We thank N. B. Ramakrishna for critical comments on the manuscript, the staff at the Gurdon Institute and the sequencing facilities at the Cancer Research UK (CRUK) Cambridge Institute, Wellcome Gurdon and Wellcome Sanger Institutes, and Genomics facility at the University of Bristol for their expertise and support. This work was supported by the following grants to E.A.M.: Wellcome Trust Senior Investigator award (nos. 104640/Z/14/Z and 219475/Z/19/Z) and CRUK award (no. C13474/A27826); to R.D.: Wellcome award (no. WT207492); to G.F.T.: Leverhulme Trust Award no. RPG-2014-214; to M.J.G., G.F.T. and B.P.N.: the Leverhulme Trust – Royal Society Africa Awards (nos. AA100023 and AA130107); to M.J.G. and G.F.T.: Natural Environment Research Council (NERC) award (no. NE/S001794/1); to M.J.G.: Leverhulme Trust award (no. RF-2014-686); to A.G.H.: Marie Skłodowska-Curie Individual Fellowship (no. GA-659791). G.V. acknowledges Wolfson College, University of Cambridge, and the Genetics Society, London, for financial support. M.E.S. is supported by an NERC Independent Research Fellowship no. NE/R01504X/1. The authors also acknowledge core funding to the Gurdon Institute from Wellcome (nos. 092096/Z/10/Z, 203144/Z/16/Z) and CRUK (no. C6946/A24843). For open access, the authors have applied a CC BY public copyright licence to any author-accepted manuscript version arising from this submission. Funding Information: We thank the staff of the Tanzania Fisheries Research Institute for their assistance and support. The Tanzania Commission for Science and Technology provided research permits and the Tanzania Ministry of Livestock and Fisheries provided export permits. We thank M. Ndawala (TAFIRI) and G. Kazumbe for their help with sample collection, and J. Johnson for her fish paintings. We thank N. B. Ramakrishna for critical comments on the manuscript, the staff at the Gurdon Institute and the sequencing facilities at the Cancer Research UK (CRUK) Cambridge Institute, Wellcome Gurdon and Wellcome Sanger Institutes, and Genomics facility at the University of Bristol for their expertise and support. This work was supported by the following grants to E.A.M.: Wellcome Trust Senior Investigator award (nos. 104640/Z/14/Z and 219475/Z/19/Z) and CRUK award (no. C13474/A27826); to R.D.: Wellcome award (no. WT207492); to G.F.T.: Leverhulme Trust Award no. RPG-2014-214; to M.J.G., G.F.T. and B.P.N.: the Leverhulme Trust – Royal Society Africa Awards (nos. AA100023 and AA130107); to M.J.G. and G.F.T.: Natural Environment Research Council (NERC) award (no. NE/S001794/1); to M.J.G.: Leverhulme Trust award (no. RF-2014-686); to A.G.H.: Marie Skłodowska-Curie Individual Fellowship (no. GA-659791). G.V. acknowledges Wolfson College, University of Cambridge, and the Genetics Society, London, for financial support. M.E.S. is supported by an NERC Independent Research Fellowship no. NE/R01504X/1. The authors also acknowledge core funding to the Gurdon Institute from Wellcome (nos. 092096/Z/10/Z, 203144/Z/16/Z) and CRUK (no. C6946/A24843). For open access, the authors have applied a CC BY public copyright licence to any author-accepted manuscript version arising from this submission. Publisher Copyright: © 2022, The Author(s).

PY - 2022/10/20

Y1 - 2022/10/20

N2 - Epigenetic variation can alter transcription and promote phenotypic divergence between populations facing different environmental challenges. Here, we assess the epigenetic basis of diversification during the early stages of speciation. Specifically, we focus on the extent and functional relevance of DNA methylome divergence in the very young radiation of Astatotilapia calliptera in crater Lake Masoko, southern Tanzania. Our study focuses on two lake ecomorphs that diverged approximately 1,000 years ago and a population in the nearby river from which they separated approximately 10,000 years ago. The two lake ecomorphs show no fixed genetic differentiation, yet are characterized by different morphologies, depth preferences and diets. We report extensive genome-wide methylome divergence between the two lake ecomorphs, and between the lake and river populations, linked to key biological processes and associated with altered transcriptional activity of ecologically relevant genes. Such genes differing between lake ecomorphs include those involved in steroid metabolism, hemoglobin composition and erythropoiesis, consistent with their divergent habitat occupancy. Using a common-garden experiment, we found that global methylation profiles are often rapidly remodeled across generations but ecomorph-specific differences can be inherited. Collectively, our study suggests an epigenetic contribution to the early stages of vertebrate speciation.

AB - Epigenetic variation can alter transcription and promote phenotypic divergence between populations facing different environmental challenges. Here, we assess the epigenetic basis of diversification during the early stages of speciation. Specifically, we focus on the extent and functional relevance of DNA methylome divergence in the very young radiation of Astatotilapia calliptera in crater Lake Masoko, southern Tanzania. Our study focuses on two lake ecomorphs that diverged approximately 1,000 years ago and a population in the nearby river from which they separated approximately 10,000 years ago. The two lake ecomorphs show no fixed genetic differentiation, yet are characterized by different morphologies, depth preferences and diets. We report extensive genome-wide methylome divergence between the two lake ecomorphs, and between the lake and river populations, linked to key biological processes and associated with altered transcriptional activity of ecologically relevant genes. Such genes differing between lake ecomorphs include those involved in steroid metabolism, hemoglobin composition and erythropoiesis, consistent with their divergent habitat occupancy. Using a common-garden experiment, we found that global methylation profiles are often rapidly remodeled across generations but ecomorph-specific differences can be inherited. Collectively, our study suggests an epigenetic contribution to the early stages of vertebrate speciation.

U2 - 10.1038/s41559-022-01894-w

DO - 10.1038/s41559-022-01894-w

M3 - Article (Academic Journal)

C2 - 36266459

SN - 2397-334X

VL - 6

SP - 1940

EP - 1951

JO - Nature Ecology and Evolution

JF - Nature Ecology and Evolution

IS - 12

ER -

Epigenetic divergence during early stages of speciation in an African crater lake cichlid fish

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