Recurrent convergent evolution at amino acid residue 261 in fish rhodopsin

Jason Hill, Erik D Enbody, Mats E Pettersson, C Grace Sprehn, Dorte Bekkevold, Arild Folkvord, Linda Laikre, Gunnar Kleinau, Patrick Scheerer, Leif Andersson*

*Corresponding author for this work

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Abstract

The evolutionary process that occurs when a species colonizes a new environment provides an opportunity to explore the mechanisms underlying genetic adaptation, which is essential knowledge for understanding evolution and the maintenance of biodiversity. Atlantic herring has an estimated total breeding stock of about 1 trillion (1012) and has colonized the brackish Baltic Sea within the last 10,000 y. Minute genetic differentiation between Atlantic and Baltic herring populations at selectively neutral loci combined with this rapid adaptation to a new environment facilitated the identification of hundreds of loci underlying ecological adaptation. A major question in the field of evolutionary biology is to what extent such an adaptive process involves selection of novel mutations with large effects or genetic changes at many loci, each with a small effect on phenotype (i.e., selection on standing genetic variation). Here we show that a missense mutation in rhodopsin (Phe261Tyr) is an adaptation to the red-shifted Baltic Sea light environment. The transition from phenylalanine to tyrosine differs only by the presence of a hydroxyl moiety in the latter, but this results in an up to 10-nm red-shifted light absorbance of the receptor. Remarkably, an examination of the rhodopsin sequences from 2,056 species of fish revealed that the same missense mutation has occurred independently and been selected for during at least 20 transitions between light environments across all fish. Our results provide a spectacular example of convergent evolution and how a single amino acid change can have a major effect on ecological adaptation.
Original languageEnglish
JournalProceedings of the National Academy of Sciences of the United States of America
Volume116
Issue number37
Pages (from-to)18473-18478
ISSN0027-8424
DOIs
Publication statusPublished - 2019

Keywords

  • Adaptation
  • Convergent evolution
  • Natural selection
  • Selective sweep

Cite this

Hill, Jason ; Enbody, Erik D ; Pettersson, Mats E ; Sprehn, C Grace ; Bekkevold, Dorte ; Folkvord, Arild ; Laikre, Linda ; Kleinau, Gunnar ; Scheerer, Patrick ; Andersson, Leif. / Recurrent convergent evolution at amino acid residue 261 in fish rhodopsin. In: Proceedings of the National Academy of Sciences of the United States of America. 2019 ; Vol. 116, No. 37. pp. 18473-18478.
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abstract = "The evolutionary process that occurs when a species colonizes a new environment provides an opportunity to explore the mechanisms underlying genetic adaptation, which is essential knowledge for understanding evolution and the maintenance of biodiversity. Atlantic herring has an estimated total breeding stock of about 1 trillion (1012) and has colonized the brackish Baltic Sea within the last 10,000 y. Minute genetic differentiation between Atlantic and Baltic herring populations at selectively neutral loci combined with this rapid adaptation to a new environment facilitated the identification of hundreds of loci underlying ecological adaptation. A major question in the field of evolutionary biology is to what extent such an adaptive process involves selection of novel mutations with large effects or genetic changes at many loci, each with a small effect on phenotype (i.e., selection on standing genetic variation). Here we show that a missense mutation in rhodopsin (Phe261Tyr) is an adaptation to the red-shifted Baltic Sea light environment. The transition from phenylalanine to tyrosine differs only by the presence of a hydroxyl moiety in the latter, but this results in an up to 10-nm red-shifted light absorbance of the receptor. Remarkably, an examination of the rhodopsin sequences from 2,056 species of fish revealed that the same missense mutation has occurred independently and been selected for during at least 20 transitions between light environments across all fish. Our results provide a spectacular example of convergent evolution and how a single amino acid change can have a major effect on ecological adaptation.",
keywords = "Adaptation, Convergent evolution, Natural selection, Selective sweep",
author = "Jason Hill and Enbody, {Erik D} and Pettersson, {Mats E} and Sprehn, {C Grace} and Dorte Bekkevold and Arild Folkvord and Linda Laikre and Gunnar Kleinau and Patrick Scheerer and Leif Andersson",
year = "2019",
doi = "10.1073/pnas.1908332116",
language = "English",
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Hill, J, Enbody, ED, Pettersson, ME, Sprehn, CG, Bekkevold, D, Folkvord, A, Laikre, L, Kleinau, G, Scheerer, P & Andersson, L 2019, 'Recurrent convergent evolution at amino acid residue 261 in fish rhodopsin', Proceedings of the National Academy of Sciences of the United States of America, vol. 116, no. 37, pp. 18473-18478. https://doi.org/10.1073/pnas.1908332116

Recurrent convergent evolution at amino acid residue 261 in fish rhodopsin. / Hill, Jason; Enbody, Erik D; Pettersson, Mats E; Sprehn, C Grace; Bekkevold, Dorte; Folkvord, Arild; Laikre, Linda; Kleinau, Gunnar; Scheerer, Patrick; Andersson, Leif.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 116, No. 37, 2019, p. 18473-18478.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Recurrent convergent evolution at amino acid residue 261 in fish rhodopsin

AU - Hill, Jason

AU - Enbody, Erik D

AU - Pettersson, Mats E

AU - Sprehn, C Grace

AU - Bekkevold, Dorte

AU - Folkvord, Arild

AU - Laikre, Linda

AU - Kleinau, Gunnar

AU - Scheerer, Patrick

AU - Andersson, Leif

PY - 2019

Y1 - 2019

N2 - The evolutionary process that occurs when a species colonizes a new environment provides an opportunity to explore the mechanisms underlying genetic adaptation, which is essential knowledge for understanding evolution and the maintenance of biodiversity. Atlantic herring has an estimated total breeding stock of about 1 trillion (1012) and has colonized the brackish Baltic Sea within the last 10,000 y. Minute genetic differentiation between Atlantic and Baltic herring populations at selectively neutral loci combined with this rapid adaptation to a new environment facilitated the identification of hundreds of loci underlying ecological adaptation. A major question in the field of evolutionary biology is to what extent such an adaptive process involves selection of novel mutations with large effects or genetic changes at many loci, each with a small effect on phenotype (i.e., selection on standing genetic variation). Here we show that a missense mutation in rhodopsin (Phe261Tyr) is an adaptation to the red-shifted Baltic Sea light environment. The transition from phenylalanine to tyrosine differs only by the presence of a hydroxyl moiety in the latter, but this results in an up to 10-nm red-shifted light absorbance of the receptor. Remarkably, an examination of the rhodopsin sequences from 2,056 species of fish revealed that the same missense mutation has occurred independently and been selected for during at least 20 transitions between light environments across all fish. Our results provide a spectacular example of convergent evolution and how a single amino acid change can have a major effect on ecological adaptation.

AB - The evolutionary process that occurs when a species colonizes a new environment provides an opportunity to explore the mechanisms underlying genetic adaptation, which is essential knowledge for understanding evolution and the maintenance of biodiversity. Atlantic herring has an estimated total breeding stock of about 1 trillion (1012) and has colonized the brackish Baltic Sea within the last 10,000 y. Minute genetic differentiation between Atlantic and Baltic herring populations at selectively neutral loci combined with this rapid adaptation to a new environment facilitated the identification of hundreds of loci underlying ecological adaptation. A major question in the field of evolutionary biology is to what extent such an adaptive process involves selection of novel mutations with large effects or genetic changes at many loci, each with a small effect on phenotype (i.e., selection on standing genetic variation). Here we show that a missense mutation in rhodopsin (Phe261Tyr) is an adaptation to the red-shifted Baltic Sea light environment. The transition from phenylalanine to tyrosine differs only by the presence of a hydroxyl moiety in the latter, but this results in an up to 10-nm red-shifted light absorbance of the receptor. Remarkably, an examination of the rhodopsin sequences from 2,056 species of fish revealed that the same missense mutation has occurred independently and been selected for during at least 20 transitions between light environments across all fish. Our results provide a spectacular example of convergent evolution and how a single amino acid change can have a major effect on ecological adaptation.

KW - Adaptation

KW - Convergent evolution

KW - Natural selection

KW - Selective sweep

U2 - 10.1073/pnas.1908332116

DO - 10.1073/pnas.1908332116

M3 - Journal article

C2 - 31451650

VL - 116

SP - 18473

EP - 18478

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 37

ER -