publication . Article . 2018

Insertions and deletions trigger adaptive walks in Drosophila proteins

Evgeny V. Leushkin; Georgii A. Bazykin; Alexey S. Kondrashov;
Open Access English
  • Published: 13 Nov 2018 Journal: Proceedings of the Royal Society B: Biological Sciences, volume 279, issue 1,740, pages 3,075-3,082 (issn: 0962-8452, eissn: 1471-2954, Copyright policy)
  • Publisher: The Royal Society
Abstract
Maps that relate all possible genotypes or phenotypes to fitness—fitness landscapes—are central to the evolution of life, but remain poorly known. An insertion or a deletion (indel) of one or several amino acids constitutes a substantial leap of a protein within the space of amino acid sequences, and it is unlikely that after such a leap the new sequence corresponds precisely to a fitness peak. Thus, one can expect an indel in the protein-coding sequence that gets fixed in a population to be followed by some number of adaptive amino acid substitutions, which move the new sequence towards a nearby fitness peak. Here, we study substitutions that occur after a fram...
Subjects
Medical Subject Headings: food and beverages
free text keywords: 1001, 70, Research Articles, indels, fitness landscape, adaptive walk, McDonald–Kreitman, General Biochemistry, Genetics and Molecular Biology, General Immunology and Microbiology, General Agricultural and Biological Sciences, General Environmental Science, General Medicine, Drosophila melanogaster, biology.organism_classification, biology, Genetics, Amino acid, chemistry.chemical_classification, chemistry, Drosophila Protein, Peptide sequence, Phenotype, Indel, Population, education.field_of_study, education
28 references, page 1 of 2

1 Kauffman S.Levin S.1987 Towards a general theory of adaptive walks on rugged landscapes. J. Theor. Biol.128, 11–45 10.1016/S0022-5193(87)80029-2 (doi:10.1016/S0022-5193(87)80029-2)3431131 [PubMed] [DOI]

2 Gillespie J. H.1984 Molecular evolution over the mutational landscape. Evolution 38, 1116–1129 10.2307/2408444 (doi:10.2307/2408444) [OpenAIRE] [DOI]

3 Orr H. A.2005 The genetic theory of adaptation: a brief history. Nat. Rev. Genet.6, 119–127 10.1038/nrg1523 (doi:10.1038/nrg1523)15716908 [OpenAIRE] [PubMed] [DOI]

4 Orr H. A.2009 Fitness and its role in evolutionary genetics. Nat. Rev. Genet.10, 531–539 10.1038/nrg2603 (doi:10.1038/nrg2603)19546856 [OpenAIRE] [PubMed] [DOI]

5 Kryazhimskiy S.Tkacik G.Plotkin J. B.2009 The dynamics of adaptation on correlated fitness landscapes. Proc. Natl Acad. Sci. USA 106, 18 638–18 643 10.1073/pnas.0905497106 (doi:10.1073/pnas.0905497106)19106304 [OpenAIRE] [PubMed] [DOI]

6 Maynard Smith J.1970 Natural selection and the concept of a protein space. Nature 225, 563–564 10.1038/225563a0 (doi:10.1038/225563a0)5411867 [OpenAIRE] [PubMed] [DOI]

7 Romero P. A.Arnold F. H.2009 Exploring protein fitness landscapes by directed evolution. Nat. Rev. Mol. Cell Biol.10, 866–876 10.1038/nrm2805 (doi:10.1038/nrm2805)19935669 [OpenAIRE] [PubMed] [DOI]

8 Gillespie J. H.1994 The causes of molecular evolution. Oxford, UK: Oxford University Press

9 Orr H. A.2003 A minimum on the mean number of steps taken in adaptiv e walks. J. Theor. Biol.220, 241–247 10.1006/jtbi.2003.3161 (doi:10.1006/jtbi.2003.3161)12468295 [OpenAIRE] [PubMed] [DOI]

10 Orr H. A.2006 The population genetics of adaptation on correlated fitness landscapes: the block model. Evolution 60, 1113–1124 16892963 [PubMed]

11 Meer M. V.Kondrashov A. S.Artzy-Randrup Y.Kondrashov F. A.2010 Compensatory evolution in mitochondrial tRNAs navigates valleys of low fitness. Nature 464, 279–282 10.1038/nature08691 (doi:10.1038/nature08691)20182427 [OpenAIRE] [PubMed] [DOI]

12 Weinreich D. M.Delaney N. F.Depristo M. A.Hartl D. L.2006 Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312, 111–114 10.1126/science.1123539 (doi:10.1126/science.1123539)16601193 [OpenAIRE] [PubMed] [DOI]

13 Wolf J. B.Brodie E. D.III Wade M. J.2000 Epistasis and the evolutionary process, 1st edn Oxford, UK: Oxford University Press

14 McDonald J. H.Kreitman M.1991 Adaptive protein evolution at the Adh locus in Drosophila. Nature 351, 652–654 10.1038/351652a0 (doi:10.1038/351652a0)1904993 [OpenAIRE] [PubMed] [DOI]

15 Smith N. G. C.Eyre-Walker A.2002 Adaptive protein evolution in Drosophila. Nature 415, 1022–1024 10.1038/4151022a (doi:10.1038/4151022a)11875568 [OpenAIRE] [PubMed] [DOI]

28 references, page 1 of 2
Abstract
Maps that relate all possible genotypes or phenotypes to fitness—fitness landscapes—are central to the evolution of life, but remain poorly known. An insertion or a deletion (indel) of one or several amino acids constitutes a substantial leap of a protein within the space of amino acid sequences, and it is unlikely that after such a leap the new sequence corresponds precisely to a fitness peak. Thus, one can expect an indel in the protein-coding sequence that gets fixed in a population to be followed by some number of adaptive amino acid substitutions, which move the new sequence towards a nearby fitness peak. Here, we study substitutions that occur after a fram...
Subjects
Medical Subject Headings: food and beverages
free text keywords: 1001, 70, Research Articles, indels, fitness landscape, adaptive walk, McDonald–Kreitman, General Biochemistry, Genetics and Molecular Biology, General Immunology and Microbiology, General Agricultural and Biological Sciences, General Environmental Science, General Medicine, Drosophila melanogaster, biology.organism_classification, biology, Genetics, Amino acid, chemistry.chemical_classification, chemistry, Drosophila Protein, Peptide sequence, Phenotype, Indel, Population, education.field_of_study, education
28 references, page 1 of 2

1 Kauffman S.Levin S.1987 Towards a general theory of adaptive walks on rugged landscapes. J. Theor. Biol.128, 11–45 10.1016/S0022-5193(87)80029-2 (doi:10.1016/S0022-5193(87)80029-2)3431131 [PubMed] [DOI]

2 Gillespie J. H.1984 Molecular evolution over the mutational landscape. Evolution 38, 1116–1129 10.2307/2408444 (doi:10.2307/2408444) [OpenAIRE] [DOI]

3 Orr H. A.2005 The genetic theory of adaptation: a brief history. Nat. Rev. Genet.6, 119–127 10.1038/nrg1523 (doi:10.1038/nrg1523)15716908 [OpenAIRE] [PubMed] [DOI]

4 Orr H. A.2009 Fitness and its role in evolutionary genetics. Nat. Rev. Genet.10, 531–539 10.1038/nrg2603 (doi:10.1038/nrg2603)19546856 [OpenAIRE] [PubMed] [DOI]

5 Kryazhimskiy S.Tkacik G.Plotkin J. B.2009 The dynamics of adaptation on correlated fitness landscapes. Proc. Natl Acad. Sci. USA 106, 18 638–18 643 10.1073/pnas.0905497106 (doi:10.1073/pnas.0905497106)19106304 [OpenAIRE] [PubMed] [DOI]

6 Maynard Smith J.1970 Natural selection and the concept of a protein space. Nature 225, 563–564 10.1038/225563a0 (doi:10.1038/225563a0)5411867 [OpenAIRE] [PubMed] [DOI]

7 Romero P. A.Arnold F. H.2009 Exploring protein fitness landscapes by directed evolution. Nat. Rev. Mol. Cell Biol.10, 866–876 10.1038/nrm2805 (doi:10.1038/nrm2805)19935669 [OpenAIRE] [PubMed] [DOI]

8 Gillespie J. H.1994 The causes of molecular evolution. Oxford, UK: Oxford University Press

9 Orr H. A.2003 A minimum on the mean number of steps taken in adaptiv e walks. J. Theor. Biol.220, 241–247 10.1006/jtbi.2003.3161 (doi:10.1006/jtbi.2003.3161)12468295 [OpenAIRE] [PubMed] [DOI]

10 Orr H. A.2006 The population genetics of adaptation on correlated fitness landscapes: the block model. Evolution 60, 1113–1124 16892963 [PubMed]

11 Meer M. V.Kondrashov A. S.Artzy-Randrup Y.Kondrashov F. A.2010 Compensatory evolution in mitochondrial tRNAs navigates valleys of low fitness. Nature 464, 279–282 10.1038/nature08691 (doi:10.1038/nature08691)20182427 [OpenAIRE] [PubMed] [DOI]

12 Weinreich D. M.Delaney N. F.Depristo M. A.Hartl D. L.2006 Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312, 111–114 10.1126/science.1123539 (doi:10.1126/science.1123539)16601193 [OpenAIRE] [PubMed] [DOI]

13 Wolf J. B.Brodie E. D.III Wade M. J.2000 Epistasis and the evolutionary process, 1st edn Oxford, UK: Oxford University Press

14 McDonald J. H.Kreitman M.1991 Adaptive protein evolution at the Adh locus in Drosophila. Nature 351, 652–654 10.1038/351652a0 (doi:10.1038/351652a0)1904993 [OpenAIRE] [PubMed] [DOI]

15 Smith N. G. C.Eyre-Walker A.2002 Adaptive protein evolution in Drosophila. Nature 415, 1022–1024 10.1038/4151022a (doi:10.1038/4151022a)11875568 [OpenAIRE] [PubMed] [DOI]

28 references, page 1 of 2
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publication . Article . 2018

Insertions and deletions trigger adaptive walks in Drosophila proteins

Evgeny V. Leushkin; Georgii A. Bazykin; Alexey S. Kondrashov;