DOI: 10.1126/science.272.5269.1802. Punctuated Evolution Caused by Selection of Rare Beneficial Mutations

Punctuated Evolution Caused by Selection of Rare Beneficial Mutations

10.1126/science.272.5269.1802

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

For more than two decades there has been intense debate over the hypothesis that most morphological evolution occurs during relatively brief episodes of rapid change that punctuate much longer periods of stasis. A clear and unambiguous case of punctuated evolution is presented for cell size in a population of Escherichia coli evolving for 3000 generations in a constant environment. The punctuation is caused by natural selection as rare, beneficial mutations sweep successively through the population. This experiment shows that the most elementary processes in population genetics can give rise to punctuated evolutionary dynamics.

Bibliography

Elena, S. F., Cooper, V. S., & Lenski, R. E. (1996). Punctuated Evolution Caused by Selection of Rare Beneficial Mutations. Science, 272(5269), 1802â1804.

Authors 3

Santiago F. Elena (first)
Vaughn S. Cooper (additional)
Richard E. Lenski (additional)

References 25 Referenced 218

ARNOLD S.J., MORPHOLOGY, PERFORMANCE AND FITNESS, AMERICAN ZOOLOGIST 23, 347 (1983). (10.1093/icb/23.2.347) / AMERICAN ZOOLOGIST / MORPHOLOGY, PERFORMANCE AND FITNESS by ARNOLD S.J. (1983)
BOOKSTEIN F.L., HIERARCHICAL LINEAR MODELING OF TEMPO AND MODE OF EVOLUTION, PALEOBIOLOGY 4, 120 (1978). (10.1017/S0094837300005807) / PALEOBIOLOGY / HIERARCHICAL LINEAR MODELING OF TEMPO AND MODE OF EVOLUTION by BOOKSTEIN F.L. (1978)
CHARLESWORTH B, A NEO-DARWINIAN COMMENTARY ON MACROEVOLUTION, EVOLUTION 36, 474 (1982). / EVOLUTION / A NEO-DARWINIAN COMMENTARY ON MACROEVOLUTION by CHARLESWORTH B (1982)
DRAKE J.W., A CONSTANT RATE OF SPONTANEOUS MUTATION IN DNA-BASED MICROBES, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 88, 7160 (1991). (10.1073/pnas.88.16.7160) / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA / A CONSTANT RATE OF SPONTANEOUS MUTATION IN DNA-BASED MICROBES by DRAKE J.W. (1991)
DYKHUIZEN D.E., SELECTION IN CHEMOSTATS, MICROBIOLOGICAL REVIEWS 47, 150 (1983). (10.1128/mr.47.2.150-168.1983) / MICROBIOLOGICAL REVIEWS / SELECTION IN CHEMOSTATS by DYKHUIZEN D.E. (1983)
ELDREDGE N, MODELS PALEOBIOLOGY: 82 (1972). / MODELS PALEOBIOLOGY by ELDREDGE N (1972)
FALCONER D.S., INTRO QUANTITATIVE G (1981). / INTRO QUANTITATIVE G by FALCONER D.S. (1981)
10.1126/science.222.4620.159
GINGERICH P.D., PUNCTUATED EQUILIBRIA - WHERE IS THE EVIDENCE, SYSTEMATIC ZOOLOGY 33, 335 (1984). (10.2307/2413079) / SYSTEMATIC ZOOLOGY / PUNCTUATED EQUILIBRIA - WHERE IS THE EVIDENCE by GINGERICH P.D. (1984)
GINZBURG L.R., BIMODALITY OF EVOLUTIONARY RATES, PALEOBIOLOGY 7, 426 (1981). (10.1017/S0094837300025483) / PALEOBIOLOGY / BIMODALITY OF EVOLUTIONARY RATES by GINZBURG L.R. (1981)
10.1038/366223a0
GOULD S.J., PERSPECTIVES EVOLUTI: 83 (1982). / PERSPECTIVES EVOLUTI by GOULD S.J. (1982)
HALDANE JBS, A mathematical theory of natural and artificial selection, Part V: Selection and mutation.PROCEEDINGS OF THE CAMBRIDGE PHILOSOPHICAL SOCIETY 23, 838 (1927). (10.1017/S0305004100015644) / PROCEEDINGS OF THE CAMBRIDGE PHILOSOPHICAL SOCIETY / A mathematical theory of natural and artificial selection, Part V: Selection and mutation. by HALDANE JBS (1927)
JOHNSON P.A., THEORETICAL-ANALYSIS OF DIVERGENCE IN MEAN FITNESS BETWEEN INITIALLY IDENTICAL POPULATIONS, PROCEEDINGS OF THE ROYAL SOCIETY OF LONDON SERIES B-BIOLOGICAL SCIENCES 259, 125 (1995). (10.1098/rspb.1995.0019) / PROCEEDINGS OF THE ROYAL SOCIETY OF LONDON SERIES B-BIOLOGICAL SCIENCES / THEORETICAL-ANALYSIS OF DIVERGENCE IN MEAN FITNESS BETWEEN INITIALLY IDENTICAL POPULATIONS by JOHNSON P.A. (1995)
KLEINBAUM D.G., APPLIED REGRESSION A (1978). / APPLIED REGRESSION A by KLEINBAUM D.G. (1978)
LENSKI R.E., LONG-TERM EXPERIMENTAL EVOLUTION IN ESCHERICHIA-COLI .1. ADAPTATION AND DIVERGENCE DURING 2,000 GENERATIONS, AMERICAN NATURALIST 138, 1315 (1991). (10.1086/285289) / AMERICAN NATURALIST / LONG-TERM EXPERIMENTAL EVOLUTION IN ESCHERICHIA-COLI .1. ADAPTATION AND DIVERGENCE DURING 2,000 GENERATIONS by LENSKI R.E. (1991)
LENSKI R.E., DYNAMICS OF ADAPTATION AND DIVERSIFICATION - A 10,000-GENERATION EXPERIMENT WITH BACTERIAL-POPULATIONS, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 91, 6808 (1994). (10.1073/pnas.91.15.6808) / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA / DYNAMICS OF ADAPTATION AND DIVERSIFICATION - A 10,000-GENERATION EXPERIMENT WITH BACTERIAL-POPULATIONS by LENSKI R.E. (1994)
LEVINTON J, GENETICS PALEONTOLOG (1988). / GENETICS PALEONTOLOG by LEVINTON J (1988)
MULLER H.J., Some genetic aspects of sex, AMERICAN NATURALIST 66, 118 (1932). (10.1086/280418) / AMERICAN NATURALIST / Some genetic aspects of sex by MULLER H.J. (1932)
NEIDHARDT F.C., PHYSL BACTERIAL CELL (1990). / PHYSL BACTERIAL CELL by NEIDHARDT F.C. (1990)
NEWMAN C.M., NEO-DARWINIAN EVOLUTION IMPLIES PUNCTUATED EQUILIBRIA, NATURE 315, 400 (1985). (10.1038/315400a0) / NATURE / NEO-DARWINIAN EVOLUTION IMPLIES PUNCTUATED EQUILIBRIA by NEWMAN C.M. (1985)
TRAVISANO M, Long-term experimental evolution in Escherichia coli .4. Targets of selection and the specificity of adaptation, GENETICS 143, 15 (1996). (10.1093/genetics/143.1.15) / GENETICS / Long-term experimental evolution in Escherichia coli .4. Targets of selection and the specificity of adaptation by TRAVISANO M (1996)
TURNER JRG, PATTERNS PROCESSES H: 183 (1986). (10.1007/978-3-642-70831-2_10) / PATTERNS PROCESSES H by TURNER JRG (1986)
VASI F, LONG-TERM EXPERIMENTAL EVOLUTION IN ESCHERICHIA-COLI .2. CHANGES IN LIFE-HISTORY TRAITS DURING ADAPTATION TO A SEASONAL ENVIRONMENT, AMERICAN NATURALIST 144, 432 (1994). (10.1086/285685) / AMERICAN NATURALIST / LONG-TERM EXPERIMENTAL EVOLUTION IN ESCHERICHIA-COLI .2. CHANGES IN LIFE-HISTORY TRAITS DURING ADAPTATION TO A SEASONAL ENVIRONMENT by VASI F (1994)
WILLIAMSON P.G., PALEONTOLOGICAL DOCUMENTATION OF SPECIATION IN CENOZOIC MOLLUSKS FROM TURKANA BASIN, NATURE 293, 437 (1981). (10.1038/293437a0) / NATURE / PALEONTOLOGICAL DOCUMENTATION OF SPECIATION IN CENOZOIC MOLLUSKS FROM TURKANA BASIN by WILLIAMSON P.G. (1981)

Dates

Type	When
Created	18 years, 10 months ago (Oct. 27, 2006, 10:30 a.m.)
Deposited	1 year, 7 months ago (Jan. 12, 2024, 4:48 p.m.)
Indexed	3 days, 11 hours ago (Aug. 28, 2025, 8:11 a.m.)
Issued	29 years, 2 months ago (June 21, 1996)
Published	29 years, 2 months ago (June 21, 1996)
Published Print	29 years, 2 months ago (June 21, 1996)

Funders 0

None

BibTeX

@article{Elena_1996, title={Punctuated Evolution Caused by Selection of Rare Beneficial Mutations}, volume={272}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.272.5269.1802}, DOI={10.1126/science.272.5269.1802}, number={5269}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Elena, Santiago F. and Cooper, Vaughn S. and Lenski, Richard E.}, year={1996}, month=jun, pages={1802–1804} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        28
      ]
    ],
    "date-time": "2025-08-28T12:11:18Z",
    "timestamp": 1756383078979
  },
  "reference-count": 25,
  "publisher": "American Association for the Advancement of Science (AAAS)",
  "issue": "5269",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1996,
        6,
        21
      ]
    ]
  },
  "abstract": "<jats:p>\n            For more than two decades there has been intense debate over the hypothesis that most morphological evolution occurs during relatively brief episodes of rapid change that punctuate much longer periods of stasis. A clear and unambiguous case of punctuated evolution is presented for cell size in a population of\n            <jats:italic>Escherichia coli</jats:italic>\n            evolving for 3000 generations in a constant environment. The punctuation is caused by natural selection as rare, beneficial mutations sweep successively through the population. This experiment shows that the most elementary processes in population genetics can give rise to punctuated evolutionary dynamics.\n          </jats:p>",
  "DOI": "10.1126/science.272.5269.1802",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2006,
        10,
        27
      ]
    ],
    "date-time": "2006-10-27T14:30:41Z",
    "timestamp": 1161959441000
  },
  "page": "1802-1804",
  "source": "Crossref",
  "is-referenced-by-count": 218,
  "title": "Punctuated Evolution Caused by Selection of Rare Beneficial Mutations",
  "prefix": "10.1126",
  "volume": "272",
  "author": [
    {
      "given": "Santiago F.",
      "family": "Elena",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Center for Microbial Ecology, Michigan State University, East Lansing, MI 48824, USA."
        }
      ]
    },
    {
      "given": "Vaughn S.",
      "family": "Cooper",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Center for Microbial Ecology, Michigan State University, East Lansing, MI 48824, USA."
        }
      ]
    },
    {
      "given": "Richard E.",
      "family": "Lenski",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Center for Microbial Ecology, Michigan State University, East Lansing, MI 48824, USA."
        }
      ]
    }
  ],
  "member": "221",
  "reference": [
    {
      "key": "e_1_2_1_2_2",
      "doi-asserted-by": "crossref",
      "first-page": "347",
      "DOI": "10.1093/icb/23.2.347",
      "article-title": "MORPHOLOGY, PERFORMANCE AND FITNESS",
      "volume": "23",
      "author": "ARNOLD S.J.",
      "year": "1983",
      "unstructured": "ARNOLD S.J., MORPHOLOGY, PERFORMANCE AND FITNESS, AMERICAN ZOOLOGIST 23, 347 (1983).",
      "journal-title": "AMERICAN ZOOLOGIST"
    },
    {
      "key": "e_1_2_1_3_2",
      "doi-asserted-by": "crossref",
      "first-page": "120",
      "DOI": "10.1017/S0094837300005807",
      "article-title": "HIERARCHICAL LINEAR MODELING OF TEMPO AND MODE OF EVOLUTION",
      "volume": "4",
      "author": "BOOKSTEIN F.L.",
      "year": "1978",
      "unstructured": "BOOKSTEIN F.L., HIERARCHICAL LINEAR MODELING OF TEMPO AND MODE OF EVOLUTION, PALEOBIOLOGY 4, 120 (1978).",
      "journal-title": "PALEOBIOLOGY"
    },
    {
      "key": "e_1_2_1_4_2",
      "first-page": "474",
      "article-title": "A NEO-DARWINIAN COMMENTARY ON MACROEVOLUTION",
      "volume": "36",
      "author": "CHARLESWORTH B",
      "year": "1982",
      "unstructured": "CHARLESWORTH B, A NEO-DARWINIAN COMMENTARY ON MACROEVOLUTION, EVOLUTION 36, 474 (1982).",
      "journal-title": "EVOLUTION"
    },
    {
      "key": "e_1_2_1_5_2",
      "doi-asserted-by": "crossref",
      "first-page": "7160",
      "DOI": "10.1073/pnas.88.16.7160",
      "article-title": "A CONSTANT RATE OF SPONTANEOUS MUTATION IN DNA-BASED MICROBES",
      "volume": "88",
      "author": "DRAKE J.W.",
      "year": "1991",
      "unstructured": "DRAKE J.W., A CONSTANT RATE OF SPONTANEOUS MUTATION IN DNA-BASED MICROBES, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 88, 7160 (1991).",
      "journal-title": "PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA"
    },
    {
      "key": "e_1_2_1_6_2",
      "doi-asserted-by": "crossref",
      "first-page": "150",
      "DOI": "10.1128/mr.47.2.150-168.1983",
      "article-title": "SELECTION IN CHEMOSTATS",
      "volume": "47",
      "author": "DYKHUIZEN D.E.",
      "year": "1983",
      "unstructured": "DYKHUIZEN D.E., SELECTION IN CHEMOSTATS, MICROBIOLOGICAL REVIEWS 47, 150 (1983).",
      "journal-title": "MICROBIOLOGICAL REVIEWS"
    },
    {
      "key": "e_1_2_1_7_2",
      "first-page": "82",
      "author": "ELDREDGE N",
      "year": "1972",
      "unstructured": "ELDREDGE N, MODELS PALEOBIOLOGY: 82 (1972).",
      "journal-title": "MODELS PALEOBIOLOGY"
    },
    {
      "key": "e_1_2_1_8_2",
      "author": "FALCONER D.S.",
      "year": "1981",
      "unstructured": "FALCONER D.S., INTRO QUANTITATIVE G (1981).",
      "journal-title": "INTRO QUANTITATIVE G"
    },
    {
      "key": "e_1_2_1_9_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.222.4620.159"
    },
    {
      "key": "e_1_2_1_10_2",
      "doi-asserted-by": "crossref",
      "first-page": "335",
      "DOI": "10.2307/2413079",
      "article-title": "PUNCTUATED EQUILIBRIA - WHERE IS THE EVIDENCE",
      "volume": "33",
      "author": "GINGERICH P.D.",
      "year": "1984",
      "unstructured": "GINGERICH P.D., PUNCTUATED EQUILIBRIA - WHERE IS THE EVIDENCE, SYSTEMATIC ZOOLOGY 33, 335 (1984).",
      "journal-title": "SYSTEMATIC ZOOLOGY"
    },
    {
      "key": "e_1_2_1_11_2",
      "doi-asserted-by": "crossref",
      "first-page": "426",
      "DOI": "10.1017/S0094837300025483",
      "article-title": "BIMODALITY OF EVOLUTIONARY RATES",
      "volume": "7",
      "author": "GINZBURG L.R.",
      "year": "1981",
      "unstructured": "GINZBURG L.R., BIMODALITY OF EVOLUTIONARY RATES, PALEOBIOLOGY 7, 426 (1981).",
      "journal-title": "PALEOBIOLOGY"
    },
    {
      "key": "e_1_2_1_12_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/366223a0"
    },
    {
      "key": "e_1_2_1_13_2",
      "first-page": "83",
      "author": "GOULD S.J.",
      "year": "1982",
      "unstructured": "GOULD S.J., PERSPECTIVES EVOLUTI: 83 (1982).",
      "journal-title": "PERSPECTIVES EVOLUTI"
    },
    {
      "key": "e_1_2_1_14_2",
      "doi-asserted-by": "crossref",
      "first-page": "838",
      "DOI": "10.1017/S0305004100015644",
      "article-title": "A mathematical theory of natural and artificial selection, Part V: Selection and mutation.",
      "volume": "23",
      "author": "HALDANE JBS",
      "year": "1927",
      "unstructured": "HALDANE JBS, A mathematical theory of natural and artificial selection, Part V: Selection and mutation.PROCEEDINGS OF THE CAMBRIDGE PHILOSOPHICAL SOCIETY 23, 838 (1927).",
      "journal-title": "PROCEEDINGS OF THE CAMBRIDGE PHILOSOPHICAL SOCIETY"
    },
    {
      "key": "e_1_2_1_15_2",
      "doi-asserted-by": "crossref",
      "first-page": "125",
      "DOI": "10.1098/rspb.1995.0019",
      "article-title": "THEORETICAL-ANALYSIS OF DIVERGENCE IN MEAN FITNESS BETWEEN INITIALLY IDENTICAL POPULATIONS",
      "volume": "259",
      "author": "JOHNSON P.A.",
      "year": "1995",
      "unstructured": "JOHNSON P.A., THEORETICAL-ANALYSIS OF DIVERGENCE IN MEAN FITNESS BETWEEN INITIALLY IDENTICAL POPULATIONS, PROCEEDINGS OF THE ROYAL SOCIETY OF LONDON SERIES B-BIOLOGICAL SCIENCES 259, 125 (1995).",
      "journal-title": "PROCEEDINGS OF THE ROYAL SOCIETY OF LONDON SERIES B-BIOLOGICAL SCIENCES"
    },
    {
      "key": "e_1_2_1_16_2",
      "author": "KLEINBAUM D.G.",
      "year": "1978",
      "unstructured": "KLEINBAUM D.G., APPLIED REGRESSION A (1978).",
      "journal-title": "APPLIED REGRESSION A"
    },
    {
      "key": "e_1_2_1_17_2",
      "doi-asserted-by": "crossref",
      "first-page": "1315",
      "DOI": "10.1086/285289",
      "article-title": "LONG-TERM EXPERIMENTAL EVOLUTION IN ESCHERICHIA-COLI .1. ADAPTATION AND DIVERGENCE DURING 2,000 GENERATIONS",
      "volume": "138",
      "author": "LENSKI R.E.",
      "year": "1991",
      "unstructured": "LENSKI R.E., LONG-TERM EXPERIMENTAL EVOLUTION IN ESCHERICHIA-COLI .1. ADAPTATION AND DIVERGENCE DURING 2,000 GENERATIONS, AMERICAN NATURALIST 138, 1315 (1991).",
      "journal-title": "AMERICAN NATURALIST"
    },
    {
      "key": "e_1_2_1_18_2",
      "doi-asserted-by": "crossref",
      "first-page": "6808",
      "DOI": "10.1073/pnas.91.15.6808",
      "article-title": "DYNAMICS OF ADAPTATION AND DIVERSIFICATION - A 10,000-GENERATION EXPERIMENT WITH BACTERIAL-POPULATIONS",
      "volume": "91",
      "author": "LENSKI R.E.",
      "year": "1994",
      "unstructured": "LENSKI R.E., DYNAMICS OF ADAPTATION AND DIVERSIFICATION - A 10,000-GENERATION EXPERIMENT WITH BACTERIAL-POPULATIONS, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 91, 6808 (1994).",
      "journal-title": "PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA"
    },
    {
      "key": "e_1_2_1_19_2",
      "author": "LEVINTON J",
      "year": "1988",
      "unstructured": "LEVINTON J, GENETICS PALEONTOLOG (1988).",
      "journal-title": "GENETICS PALEONTOLOG"
    },
    {
      "key": "e_1_2_1_20_2",
      "doi-asserted-by": "crossref",
      "first-page": "118",
      "DOI": "10.1086/280418",
      "article-title": "Some genetic aspects of sex",
      "volume": "66",
      "author": "MULLER H.J.",
      "year": "1932",
      "unstructured": "MULLER H.J., Some genetic aspects of sex, AMERICAN NATURALIST 66, 118 (1932).",
      "journal-title": "AMERICAN NATURALIST"
    },
    {
      "key": "e_1_2_1_21_2",
      "author": "NEIDHARDT F.C.",
      "year": "1990",
      "unstructured": "NEIDHARDT F.C., PHYSL BACTERIAL CELL (1990).",
      "journal-title": "PHYSL BACTERIAL CELL"
    },
    {
      "key": "e_1_2_1_22_2",
      "doi-asserted-by": "crossref",
      "first-page": "400",
      "DOI": "10.1038/315400a0",
      "article-title": "NEO-DARWINIAN EVOLUTION IMPLIES PUNCTUATED EQUILIBRIA",
      "volume": "315",
      "author": "NEWMAN C.M.",
      "year": "1985",
      "unstructured": "NEWMAN C.M., NEO-DARWINIAN EVOLUTION IMPLIES PUNCTUATED EQUILIBRIA, NATURE 315, 400 (1985).",
      "journal-title": "NATURE"
    },
    {
      "key": "e_1_2_1_23_2",
      "doi-asserted-by": "crossref",
      "first-page": "15",
      "DOI": "10.1093/genetics/143.1.15",
      "article-title": "Long-term experimental evolution in Escherichia coli .4. Targets of selection and the specificity of adaptation",
      "volume": "143",
      "author": "TRAVISANO M",
      "year": "1996",
      "unstructured": "TRAVISANO M, Long-term experimental evolution in Escherichia coli .4. Targets of selection and the specificity of adaptation, GENETICS 143, 15 (1996).",
      "journal-title": "GENETICS"
    },
    {
      "key": "e_1_2_1_24_2",
      "doi-asserted-by": "crossref",
      "first-page": "183",
      "DOI": "10.1007/978-3-642-70831-2_10",
      "author": "TURNER JRG",
      "year": "1986",
      "unstructured": "TURNER JRG, PATTERNS PROCESSES H: 183 (1986).",
      "journal-title": "PATTERNS PROCESSES H"
    },
    {
      "key": "e_1_2_1_25_2",
      "doi-asserted-by": "crossref",
      "first-page": "432",
      "DOI": "10.1086/285685",
      "article-title": "LONG-TERM EXPERIMENTAL EVOLUTION IN ESCHERICHIA-COLI .2. CHANGES IN LIFE-HISTORY TRAITS DURING ADAPTATION TO A SEASONAL ENVIRONMENT",
      "volume": "144",
      "author": "VASI F",
      "year": "1994",
      "unstructured": "VASI F, LONG-TERM EXPERIMENTAL EVOLUTION IN ESCHERICHIA-COLI .2. CHANGES IN LIFE-HISTORY TRAITS DURING ADAPTATION TO A SEASONAL ENVIRONMENT, AMERICAN NATURALIST 144, 432 (1994).",
      "journal-title": "AMERICAN NATURALIST"
    },
    {
      "key": "e_1_2_1_26_2",
      "doi-asserted-by": "crossref",
      "first-page": "437",
      "DOI": "10.1038/293437a0",
      "article-title": "PALEONTOLOGICAL DOCUMENTATION OF SPECIATION IN CENOZOIC MOLLUSKS FROM TURKANA BASIN",
      "volume": "293",
      "author": "WILLIAMSON P.G.",
      "year": "1981",
      "unstructured": "WILLIAMSON P.G., PALEONTOLOGICAL DOCUMENTATION OF SPECIATION IN CENOZOIC MOLLUSKS FROM TURKANA BASIN, NATURE 293, 437 (1981).",
      "journal-title": "NATURE"
    }
  ],
  "container-title": "Science",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://www.science.org/doi/pdf/10.1126/science.272.5269.1802",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2024,
        1,
        12
      ]
    ],
    "date-time": "2024-01-12T21:48:59Z",
    "timestamp": 1705096139000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.science.org/doi/10.1126/science.272.5269.1802"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1996,
        6,
        21
      ]
    ]
  },
  "references-count": 25,
  "journal-issue": {
    "issue": "5269",
    "published-print": {
      "date-parts": [
        [
          1996,
          6,
          21
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1126/science.272.5269.1802"
  ],
  "URL": "http://dx.doi.org/10.1126/science.272.5269.1802",
  "relation": {},
  "ISSN": [
    "0036-8075",
    "1095-9203"
  ],
  "subject": [],
  "container-title-short": "Science",
  "published": {
    "date-parts": [
      [
        1996,
        6,
        21
      ]
    ]
  }
}